Detecting Genetic Association of Common Human Facial Morphological Variation Using High Density 3D Image Registration

PLoS Computational Biology

Volumn 9, Issue 12, 2013, Pages

  Peng, Shouneng ^a   Tan, Jingze ^b   Hu, Sile ^a   Zhou, Hang ^a   Guo, Jing ^a   Jin, Li ^a,b   Tang, Kun ^a  

^a MAX PLANCK INSTITUTE   (Germany)

^b FUDAN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

GEOMETRY;

3D IMAGE REGISTRATION; COMPLEX TRAITS; GENETIC BASIS; GEOMETRIC ANALYSIS; IMAGES REGISTRATION; MORPHOLOGICAL VARIATION; SAMPLE FACES; SHAPE CHANGE; SIMPLE++; STATISTICAL POWER;

IMAGE REGISTRATION;

FIBROBLAST GROWTH FACTOR RECEPTOR 1; GROWTH HORMONE RECEPTOR; INTERFERON REGULATORY FACTOR 6; PHOSPHODIESTERASE I;

ADOLESCENT; ADULT; ARTICLE; CLEFT LIP; CLEFT PALATE; ENPP1 GENE; FACE PROFILE; FEMALE; FGFR1 GENE; GENETIC ASSOCIATION; GENETIC IDENTIFICATION; GENETIC RISK; GENETIC VARIABILITY; GEOMETRY; GHR GENE; HUMAN; HUMAN EXPERIMENT; IMAGE PROCESSING; IRF6 GENE; LIP; MALE; MORPHOLOGICAL TRAIT; NORMAL HUMAN; PHENOTYPE; PHENOTYPIC VARIATION; RISK FACTOR; SINGLE NUCLEOTIDE POLYMORPHISM; THREE DIMENSIONAL IMAGING; VALIDATION PROCESS; YOUNG ADULT;

FACE; HUMANS; IMAGING, THREE-DIMENSIONAL; MODELS, ANATOMIC; POLYMORPHISM, SINGLE NUCLEOTIDE;

EID: 84892705958     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1003375     Document Type: Article

References (50)

1. Johannsdottir B, Thorarinsson F, Thordarson A, Magnusson TE, (2005) Heritability of craniofacial characteristics between parents and offspring estimated from lateral cephalograms. American journal of orthodontics and dentofacial orthopedics: official publication of the American Association of Orthodontists, its constituent societies, and the American Board of Orthodontics. 127: 200-7; quiz 260-1 Available: http://www.ncbi.nlm.nih.gov/pubmed/15750539. Accessed 27 November 2012.
2. Liu F, van der Lijn F, Schurmann C, Zhu G, Chakravarty MM, et al. (2012) A Genome-Wide Association Study Identifies Five Loci Influencing Facial Morphology in Europeans. PLoS Genetics 8: e1002932 Available: http://dx.plos.org/10.1371/journal.pgen.1002932. Accessed 17 September 2012.
3. Abzhanov A, Kuo WP, Hartmann C, Grant BR, Grant PR, et al. (2006) The calmodulin pathway and evolution of elongated beak morphology in Darwin's finches. Nature 442: 563-567 Available: http://www.ncbi.nlm.nih.gov/pubmed/16885984. Accessed 16 July 2012.
4. Hubbe M, Hanihara T, Harvati K, (2009) Climate signatures in the morphological differentiation of worldwide modern human populations. Anatomical record (Hoboken, NJ: 2007) 292: 1720-1733 Available: http://www.ncbi.nlm.nih.gov/pubmed/19718714. Accessed 14 December 2012.
5. Harvati K, Weaver TD, (2006) Human cranial anatomy and the differential preservation of population history and climate signatures. The anatomical record Part A, Discoveries in molecular, cellular, and evolutionary biology 288: 1225-1233 Available: http://www.ncbi.nlm.nih.gov/pubmed/17075844. Accessed 9 November 2012.
6. Boehringer S, van der Lijn F, Liu F, Günther M, Sinigerova S, et al. (2011) Genetic determination of human facial morphology: links between cleft-lips and normal variation. European journal of human genetics: EJHG pp. 1192-1197 Available: http://www.ncbi.nlm.nih.gov/pubmed/21694738. Accessed 26 July 2011.
7. Kayser M, Schneider PM, (2009) DNA-based prediction of human externally visible characteristics in forensics: motivations, scientific challenges, and ethical considerations. Forensic science international. Genetics 3: 154-161 Available: http://www.ncbi.nlm.nih.gov/pubmed/19414162. Accessed 27 July 2011.
8. Hutton TJ, Buxton BF, Hammond P, Potts HWW, (2003) Estimating average growth trajectories in shape-space using kernel smoothing. IEEE transactions on medical imaging 22: 747-753 Available: http://www.ncbi.nlm.nih.gov/pubmed/12872950.
9. Buchtová M, Kuo WP, Nimmagadda S, Benson SL, Geetha-Loganathan P, et al. (2010) Whole genome microarray analysis of chicken embryo facial prominences. Developmental dynamics: an official publication of the American Association of Anatomists 239: 574-591 Available: http://www.ncbi.nlm.nih.gov/pubmed/19941351. Accessed 29 September 2012.
10. Cai J, Ash D, Kotch LE, Jabs EW, Attie-Bitach T, et al. (2005) Gene expression in pharyngeal arch 1 during human embryonic development. Human molecular genetics 14: 903-912 Available: http://www.ncbi.nlm.nih.gov/pubmed/15703188. Accessed 7 August 2012.
11. Chai Y, Maxson RE, (2006) Recent advances in craniofacial morphogenesis. Developmental dynamics: an official publication of the American Association of Anatomists 235: 2353-2375 Available: http://www.ncbi.nlm.nih.gov/pubmed/16680722. Accessed 27 July 2012.
12. Feng W, Simoes-de-Souza F, Finger TE, Restrepo D, Williams T, (2009) Disorganized olfactory bulb lamination in mice deficient for transcription factor AP-2epsilon. Molecular and cellular neurosciences 42: 161-171 Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2745980&tool=pmcentrez&rendertype=abstract. Accessed 14 September 2012.
13. Brugmann Sa, Goodnough LH, Gregorieff A, Leucht P, ten Berge D, et al. (2007) Wnt signaling mediates regional specification in the vertebrate face. Development (Cambridge, England) 134: 3283-3295 Available: http://www.ncbi.nlm.nih.gov/pubmed/17699607. Accessed 19 July 2012.
14. Nanni L, Ming JE, Bocian M, Steinhaus K, Bianchi DW, et al. (1999) The mutational spectrum of the sonic hedgehog gene in holoprosencephaly: SHH mutations cause a significant proportion of autosomal dominant holoprosencephaly. Human molecular genetics 8: 2479-2488 Available: http://www.ncbi.nlm.nih.gov/pubmed/10556296.
15. Kang EH, Yamaguchi T, Tajima A, Nakajima T, Tomoyasu Y, et al. (2009) Association of the growth hormone receptor gene polymorphisms with mandibular height in a Korean population. Archives of oral biology 54: 556-562 Available: http://www.ncbi.nlm.nih.gov/pubmed/19344888. Accessed 1 June 2012.
16. Weinberg SM, Naidoo SD, Bardi KM, Brandon Ca, Neiswanger K, et al. (2009) Face shape of unaffected parents with cleft affected offspring: combining three-dimensional surface imaging and geometric morphometrics. Orthodontics & craniofacial research 12: 271-281 Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2765674&tool=pmcentrez&rendertype=abstract.
17. Birnbaum S, Ku L, Reutter H, Herms S, Na DA, et al. (2009) Short communication IRF6 gene variants in Central European patients with non-syndromic cleft lip with or without cleft palate. pp. 766-769.
18. Mangold E, Ludwig KU, Birnbaum S, Baluardo C, Ferrian M, et al. (2010) Genome-wide association study identifies two susceptibility loci for nonsyndromic cleft lip with or without cleft palate. Nature genetics 42: 24-26 Available: http://www.ncbi.nlm.nih.gov/pubmed/20023658. Accessed 2 November 2012.
19. Beaty TH, Murray JC, Marazita ML, Munger RG, Ruczinski I, et al. (2010) A genome-wide association study of cleft lip with and without cleft palate identifies risk variants near MAFB and ABCA4. Nature genetics 42: 525-529 Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2941216&tool=pmcentrez&rendertype=abstract. Accessed 13 November 2012.
20. Blanton SH, Cortez A, Stal S, Mulliken JB, Finnell RH, et al. (2005) Variation in IRF6 contributes to nonsyndromic cleft lip and palate. American journal of medical genetics Part A 137A: 259-262 Available: http://www.ncbi.nlm.nih.gov/pubmed/16096995. Accessed 11 September 2012.
21. Zucchero TM, Cooper ME, Maher BS, Daack-Hirsch S, Nepomuceno B, et al. (2004) Interferon regulatory factor 6 (IRF6) gene variants and the risk of isolated cleft lip or palate. The New England journal of medicine 351: 769-780 Available: http://www.ncbi.nlm.nih.gov/pubmed/15317890.
22. Thomason HA, Zhou H, Kouwenhoven EN, Dotto G, Restivo G, et al. (2010) Cooperation between the transcription factors p63 and IRF6 is essential to prevent cleft palate in mice. J Clin Invest 120: 1561-1569 doi:10.1172/JCI40266DS1.
23. Wu T, Liang KY, Hetmanski JB, Ruczinski I, Fallin MD, et al. (2010) Evidence of gene-environment interaction for the IRF6 gene and maternal multivitamin supplementation in controlling the risk of cleft lip with/without cleft palate. Human genetics 128: 401-410 Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2956506&tool=pmcentrez&rendertype=abstract. Accessed 29 September 2012.
24. Huang Y, Wu J, Ma J, Beaty TH, Sull JW, et al. (2009) Association between IRF6 SNPs and oral clefts in West China. Journal of dental research 88: 715-718 Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2901597&tool=pmcentrez&rendertype=abstract. Accessed 29 September 2012.
25. Slavkin HC, (2001) The Human Genome, Implications for Oral Health and Diseases, and Dental Education. Journal of Dental Education pp. 463-479.
26. Shieh JTC, Aradhya S, Novelli A, Manning MA, Cherry AM, et al. (2006) Nablus Mask-Like Facial Syndrome Is Caused by a Microdeletion of 8q Detected by Array-Based Comparative Genomic Hybridization. Am J Med Genet A 140: 1267-1273 doi:10.1002/ajmg.a.
27. Gorlin RJ, (1998) Otodental syndrome, oculo-facio-cardio-dental (OFCD) syndrome, and lobodontia: dental disorders of interest to the pediatric radiologist. Pediatric radiology 28: 802-804 Available: http://www.ncbi.nlm.nih.gov/pubmed/9799305.
28. Brennan M, Pauli RM, (2001) Hajdu-Cheney syndrome: evolution of phenotype and clinical problems. American journal of medical genetics 100: 292-310 Available: http://www.ncbi.nlm.nih.gov/pubmed/11343321.
29. Riise R, Tornqvist K, Wright AF, Mykytyn K, Sheffield VC, (2002) The phenotype in Norwegian patients with Bardet-Biedl syndrome with mutations in the BBS4 gene. Archives of ophthalmology 120: 1364-1367 Available: http://www.ncbi.nlm.nih.gov/pubmed/12365916.
30. Yamaguchi T, Maki K, Shibasaki Y, (2001) Growth hormone receptor gene variant and mandibular height in the normal Japanese population. American journal of orthodontics and dentofacial orthopedics: official publication of the American Association of Orthodontists, its constituent societies, and the American Board of Orthodontics 119: 650-653 Available: http://www.ncbi.nlm.nih.gov/pubmed/11395710. Accessed 29 September 2012.
31. Tomoyasu Y, Yamaguchi T, Tajima A, Nakajima T, Inoue I, et al. (2009) Further evidence for an association between mandibular height and the growth hormone receptor gene in a Japanese population. American journal of orthodontics and dentofacial orthopedics: official publication of the American Association of Orthodontists, its constituent societies, and the American Board of Orthodontics 136: 536-541 Available: http://www.ncbi.nlm.nih.gov/pubmed/19815155. Accessed 29 September 2012.
32. Zhou J, Lu Y, Gao XH, Chen YC, Lu JJ, et al. (2005) The Growth Hormone Receptor Gene is Associated with Mandibular Height in a Chinese Population. Journal of Dental Research 84: 1052-1056 Available: http://jdr.sagepub.com/cgi/doi/10.1177/154405910508401116. Accessed 29 September 2012.
33. Ermakov S, Rosenbaum MG, Malkin I, Livshits G, (2010) Family-based study of association between ENPP1 genetic variants and craniofacial morphology. Annals of human biology 37: 754-766 Available: http://www.ncbi.nlm.nih.gov/pubmed/20446819. Accessed 29 September 2012.
34. Coussens A, Daal A (2005) Linkage disequilibrium analysis identifies an FGFR1 haplotype-tag SNP associated with normal variation in craniofacial shape. Genomics 85: 563-573. Available: http://www.sciencedirect.com/science/article/pii/S0888754305000340. Accessed 8 May 2013.
35. Paternoster L, Zhurov AI, Toma AM, Kemp JP, St Pourcain B, et al. (2012) Genome-wide Association Study of Three-Dimensional Facial Morphology Identifies a Variant in PAX3 Associated with Nasion Position. The American Journal of Human Genetics 90: 478-85.
36. Von Cramon-Taubadel N, (2009) Congruence of individual cranial bone morphology and neutral molecular affinity patterns in modern humans. American journal of physical anthropology 140: 205-215 Available: http://www.ncbi.nlm.nih.gov/pubmed/19418568. Accessed 28 October 2012.
37. Dryden IL, Mardia K V (1998) Statistical Shape Analysis. John Wiley and Sons. Available: http://linkinghub.elsevier.com/retrieve/pii/S0047248499903913.
38. Hammond P, Hutton TJ, Allanson JE, Campbell LE, Hennekam RCM, et al. (2004) 3D analysis of facial morphology. American journal of medical genetics Part A 126A: 339-348 Available: http://www.ncbi.nlm.nih.gov/pubmed/15098232. Accessed 19 March 2012.
39. Guo J, Mei X, Tang K, (2013) Automatic landmark annotation and dense correspondence registration for 3D human facial images. BMC bioinformatics 14: 232 Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3724574&tool=pmcentrez&rendertype=abstract. Accessed 7 August 2013.
40. Hammond P, (2007) The use of 3D face shape modelling in dysmorphology. Archives of disease in childhood 92: 1120-1126 Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2066088&tool=pmcentrez&rendertype=abstract. Accessed 10 September 2012.
41. Hammond P, Hannes F, Suttie M, Devriendt K, Vermeesch JR, et al. (2012) Fine-grained facial phenotype-genotype analysis in Wolf-Hirschhorn syndrome. European journal of human genetics: EJHG 20: 33-40 Available: http://www.ncbi.nlm.nih.gov/pubmed/21792232. Accessed 27 August 2012.
42. Hammond P, Suttie M, (2012) Large-scale objective phenotyping of 3D facial morphology. Human mutation 33: 817-825 Available: http://www.ncbi.nlm.nih.gov/pubmed/22434506. Accessed 4 June 2012.
43. Gómez-Valdés J a, Hünemeier T, Contini V, Acuña-Alonzo V, Macin G, et al. (2012) Fibroblast growth factor receptor 1 (FGFR1) variants and craniofacial variation in Amerindians and related populations. American journal of human biology: the official journal of the Human Biology Council 000: 1-8 Available: http://www.ncbi.nlm.nih.gov/pubmed/23070782. Accessed 4 December 2012.
44. Pan Y, Ma J, Zhang W, Du Y, Niu Y, et al. (2010) IRF6 polymorphisms are associated with nonsyndromic orofacial clefts in a Chinese Han population. American journal of medical genetics Part A 152A: 2505-2511 Available: http://www.ncbi.nlm.nih.gov/pubmed/20799332. Accessed 3 September 2012.
45. Larrabee YC, Birkeland AC, Kent DT, Flores C, Su GH, et al. (2011) Association of common variants, not rare mutations, in IRF6 With nonsyndromic clefts in a honduran population. The Laryngoscope 121: 1756-1759.
46. Park JW, McIntosh I, Hetmanski JB, Jabs EW, Vander Kolk Ca, et al. (2007) Association between IRF6 and nonsyndromic cleft lip with or without cleft palate in four populations. Genetics in Medicine 9: 219-227 Available: http://www.nature.com/doifinder/10.1097/GIM.0b013e3180423cca. Accessed 29 September 2012.
47. Vieira R, (2008) Unraveling Human Cleft Lip and Palate Research. Journal of Dental Research 87: 119-125 Available: http://jdr.sagepub.com/cgi/doi/10.1177/154405910808700202. Accessed 11 September 2012.
48. Dixon MJ, Marazita ML, Beaty TH, Murray JC, (2011) Cleft lip and palate: understanding genetic and environmental influences. Nature reviews Genetics 12: 167-178 Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3086810&tool=pmcentrez&rendertype=abstract. Accessed 4 July 2011.
49. Hoff-Olsen P, Mevåg B, Staalstrøm E, Hovde B, Egeland T, et al. (1999) Extraction of DNA from decomposed human tissue. An evaluation of five extraction methods for short tandem repeat typing. Forensic science international 105: 171-183 Available: http://www.ncbi.nlm.nih.gov/pubmed/10643651.
50. So H-C, Sham PC, (2011) Multiple testing and power calculations in genetic association studies. Cold Spring Harbor Protocols 2011: pdb-top95.