Quantitative trait loci affecting the 3D skull shape and size in mouse and prioritization of candidate genes in-silico

Frontiers in Physiology

Volumn 6, Issue MAR, 2015, Pages

  Murat Maga, A ^a,b   Navarro, Nicolas ^c,d   Cunningham, Michael L ^a,b   Cox, Timothy C ^a,b,e  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^b SEATTLE CHILDREN S RESEARCH INSTITUTE   (United States)

^c PSL RESEARCH UNIVERSITY   (France)

^d UNIVERSITÉ DE BOURGOGNE   (France)

^e MONASH UNIVERSITY   (Australia)

Author keywords

3D imaging; Candidate gene enrichment; Geometric morphometrics; Multivariate QTL mapping; Skull shape

Indexed keywords

A J MOUSE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARNTL2 GENE; ARTICLE; AUTOSOME; BACKCROSSING; BIOINFORMATICS; C57BL 6 MOUSE; CAD GENE; CD93 GENE; COL16A1 GENE; COMPUTER MODEL; CONTROLLED STUDY; CRANIOFACIAL DEVELOPMENT; CRANIOFACIAL MALFORMATION; DOK1 GENE; EFFECT SIZE; EPHA3 GENE; FCGR2B GENE; FEMALE; GCFC2 GENE; GENDER; GENE; GENE IDENTIFICATION; INBRED MOUSE STRAIN; ITGA2 GENE; KIF7 GENE; MALE; MICRO-COMPUTED TOMOGRAPHY; MORPHOMETRICS; MOUSE; NONHUMAN; PALATE; PAX1 GENE; PPARGC1B GENE; QUANTITATIVE TRAIT LOCUS; SINGLE NUCLEOTIDE POLYMORPHISM; SKULL; TAF1B GENE; TBX3 GENE; THRAP3 GENE; THREE DIMENSIONAL IMAGING;

EID: 84926479433     PISSN: None     EISSN: 1664042X     Source Type: Journal    
DOI: 10.3389/fphys.2015.00092     Document Type: Article

References (75)

1. Adams, D. C., Rohlf, F. J., and Slice, D. E. (2013). A field comes of age: geometric morphometrics in the 21st century. Hystrix Ital. J. Mammal . 24, 7-14. doi: 10.4404/hystrix-24.1-6283
2. Agrawal, P., Wang, M., Kim, S., Lewis, A. E., and Bush, J. O. (2014). Embryonic expression of EphA receptor genes in mice supports their candidacy for involvement in cleft lip and palate. Dev. Dyn . 243, 1470-1476. doi: 10.1002/dvdy.24170
3. Battaglia, A., Carey, J. C., South, S. T., and Wright, T. J. (1993). "Wolf-Hirschhorn Syndrome," in Gene Reviews(®) , eds R. A. Pagon, M. P. Adam, H. H. Ardinger, T. D. Bird, C. R. Dolan, C.-T. Fong, R. J. Smith, and K. Stephens (Seattle, WA: University of Washington). Available online at: http://www.ncbi.nlm.nih.gov/books/NBK1183/[Accessed December 23, 2014].
4. Boell, L. (2013). Lines of least resistance and genetic architecture of house mouse (Mus musculus) mandible shape. Evol. Dev . 15, 197-204. doi: 10.1111/ede.12033
5. Boell, L., Gregorova, S., Forejt, J., and Tautz, D. (2011). A comparative assessment of mandible shape in a consomic strain panel of the house mouse (Mus musculus)-implications for epistasis and evolvability of quantitative traits. BMC Evol. Biol . 11:309. doi: 10.1186/1471-2148-11-309
6. Boell, L., Pallares, L. F., Brodski, C., Chen, Y., Christian, J. L., Kousa, Y. A., et al. (2013). Exploring the effects of gene dosage on mandible shape in mice as a model for studying the genetic basis of natural variation. Dev. Genes Evol . 223, 279-287. doi: 10.1007/s00427-013-0443-y
7. Broman, K. W., Rowe, L. B., Churchill, G. A., and Paigen, K. (2002). Crossover interference in the mouse. Genetics 160, 1123-1131.
8. Broman, K. W., and Sen, S. (2009). A Guide to QTL Mapping with R/qtl . New York, NY: Springer.
9. Broman, K. W., and Speed, T. P. (2002). A model selection approach for the identification of quantitative trait loci in experimental crosses. J. R. Stat. Soc. Ser. B Stat. Methodol . 64, 641-656. doi: 10.1111/1467-9868.00354
10. Broman, K. W., Wu, H., Sen, S., and Churchill, G. A. (2003). R/qtl: QTL mapping in experimental crosses. Bioinformatics 19, 889-890. doi: 10.1093/bioinformatics/btg112
11. Burgio, G., Baylac, M., Heyer, E., and Montagutelli, X. (2009). Genetic analysis of skull shape variation and morphological integration in the mouse using interspecific recombinant congenic strains between c57bl/6 and mice of the mus spretus species. Evolution 63, 2668-2686. doi: 10.1111/j.1558-5646.2009.00737.x
12. Chen, J., Bardes, E. E., Aronow, B. J., and Jegga, A. G. (2009). ToppGene Suite for gene list enrichment analysis and candidate gene prioritization. Nucleic Acids Res . 37, W305-W311. doi: 10.1093/nar/gkp427
13. Churchill, G. A., and Doerge, R. W. (1994). Empirical threshold values for quantitative trait mapping. Genetics 138, 963-971.
14. Cox, A., Ackert-Bicknell, C. L., Dumont, B. L., Ding, Y., Bell, J. T., Brockmann, G. A., et al. (2009). A new standard genetic map for the laboratory mouse. Genetics 182, 1335-1344. doi: 10.1534/genetics.109.105486
15. Dietrich, S., Schubert, F. R., and Gruss, P. (1993). Altered Pax gene expression in murine notochord mutants: the notochord is required to initiate and maintain ventral identity in the somite. Mech. Dev . 44, 189-207.
16. Drake, A. G., and Klingenberg, C. P. (2008). The pace of morphological change: historical transformation of skull shape in St Bernard dogs. Proc. R. Soc. B Biol. Sci . 275, 71-76. doi: 10.1098/rspb.2007.1169
17. Dryden, I. L., and Mardia, K. M. (2008). Statistical Shape Analysis . Chicester: John Wiley and Sons.
18. Dupuis, J., and Siegmund, D. (1999). Statistical methods for mapping quantitative trait loci from a dense set of markers. Genetics 151, 373-386.
19. Feng, W., Leach, S. M., Tipney, H., Phang, T., Geraci, M., Spritz, R. A., et al. (2009). Spatial and temporal analysis of gene expression during growth and fusion of the mouse facial prominences. PLoS ONE 4:e8066. doi: 10.1371/journal.pone.0008066
20. Goodall, C. (1991). Procrustes methods in the statistical analysis of shape. J. R. Stat. Soc. Ser. B Methodol . 53, 285-339.
21. Hager, R., Cheverud, J. M., and Wolf, J. B. (2008). Maternal effects as the cause of parent-of-origin effects that mimic genomic imprinting. Genetics 178, 1755-1762. doi: 10.1534/genetics.107.080697
22. Haley, C., and Knott, S. (1992). A simple regression method for mapping quantitative trait loci in line crosses using flanking markers. Heredity 69, 315-324.
23. Hallgrimsson, B., Mio, W., Marcucio, R. S., and Spritz, R. (2014). Let's face it-complex traits are just not that simple. PLoS Genet 10:e1004724. doi: 10.1371/journal.pgen.1004724
24. Herring, S. (1993). "Epigenetic and functional influences on skull growth," in The Skull , eds J. Hanken and B. K. Hall (Chicago, IL: University of Chicago Press), 153-206.
25. Kendall, D. G. (1984). Shape manifolds, procrustean metrics, and complex projective spaces. Bull. Lond. Math. Soc . 16, 81-121. doi: 10.1112/blms/16.2.81
26. Kenney-Hunt, J. P., Vaughn, T. T., Pletscher, L. S., Peripato, A., Routman, E., Cothran, K., et al. (2006). Quantitative trait loci for body size components in mice. Mamm. Genome 17, 526-537. doi: 10.1007/s00335-005-0160-6
27. Kenney-Hunt, J. P., Wang, B., Norgard, E. A., Fawcett, G., Falk, D., Pletscher, L. S., et al. (2008). Pleiotropic patterns of quantitative trait loci for 70 murine skeletal traits. Genetics 178, 2275-2288. doi: 10.1534/genetics.107.084434
28. Kent, J. T., and Mardia, K. V. (1997). Consistency of procrustes estimators. J. R. Stat. Soc. Ser. B Methodol . 59, 281-290.
29. Klingenberg, C. P. (2010). Evolution and development of shape: integrating quantitative approaches. Nat. Rev. Genet . 11, 623-635. doi: 10.1038/nrg2829
30. Klingenberg, C. P. (2011). MorphoJ: an integrated software package for geometric morphometrics. Mol. Ecol. Resour . 11, 353-357. doi: 10.1111/j.1755-0998.2010.02924.x
31. Klingenberg, C. P., Barluenga, M., and Meyer, A. (2002). Shape analysis of symmetric structures: quantifying variation among individuals and asymmetry. Evolution 56, 1909-1920. doi: 10.1111/j.0014-3820.2002.tb00117.x
32. Klingenberg, C. P., Leamy, L. J., and Cheverud, J. M. (2004). Integration and modularity of quantitative trait locus effects on geometric shape in the mouse mandible. Genetics 166, 1909-1921. doi: 10.1534/genetics.166.4.1909
33. Klingenberg, C. P., Leamy, L. J., Routman, E. J., and Cheverud, J. M. (2001). Genetic architecture of mandible shape in mice: effects of quantitative trait loci analyzed by geometric morphometrics. Genetics 157, 785-802.
34. Klingenberg, C. P., and Navarro, N. (2012). "Development of the mouse mandible: a model system for complex morphological structures," in Evolution of the House Mouse , eds M. Macholán, S. J. E. Baird, P. Munclinger, and J. Piálek (Cambridge: Cambridge University Press), 135-149.
35. Knott, S. A., and Haley, C. S. (2000). Multitrait least squares for quantitative trait loci detection. Genetics 156, 899-911.
36. Lamichhaney, S., Berglund, J., Almén, M. S., Maqbool, K., Grabherr, M., Martinez-Barrio, A., et al. (2015). Evolution of Darwin's finches and their beaks revealed by genome sequencing. Nature 518, 371-375. doi: 10.1038/nature14181
37. Lander, E. S., and Botstein, D. (1989). Mapping mendelian factors underlying quantitative traits using RFLP linkage maps. Genetics 121, 185-199.
38. Laurie, C. C., Nickerson, D. A., Anderson, A. D., Weir, B. S., Livingston, R. J., Dean, M. D., et al. (2007). Linkage disequilibrium in wild mice. PLoS Genet . 3:e144. doi: 10.1371/journal.pgen.0030144
39. Leamy, L. J., Klingenberg, C. P., Sherratt, E., Wolf, J. B., and Cheverud, J. M. (2008). A search for quantitative trait loci exhibiting imprinting effects on mouse mandible size and shape. Heredity 101, 518-526. doi: 10.1038/hdy.2008.79
40. Leamy, L. J., Routman Eric, J., and Cheverud, J. M. (1999). Quantitative trait loci for early- and late-developing skull characters in mice: a test of the genetic independence model of morphological integration. Am. Nat . 153, 201-214. doi: 10.1086/303165
41. Lele, S., and Richtsmeier, J. (1990). Statistical-models in morphometrics - are they realistic. Syst. Zool . 39, 60-69. doi: 10.2307/2992208
42. Lele, S., and Richtsmeier, J. (1991). Euclidean distance matrix analysis - a coordinate-free approach for comparing biological shapes using landmark data. Am. J. Phys. Anthropol . 86, 415-427. doi: 10.1002/ajpa.1330860307
43. Lieberman, D. E. (2011). "Epigenetic integration, complexity, and the evolvability of the head: Re-thinking the functional matrix hypothesis," in, eds B. Hallgrimsson and B. K. Hall (Berkeley, CA: University of California Press).
44. Liu, F., van der Lijn, F., Schurmann, C., Zhu, G., Chakravarty, M. M., Hysi, P. G., et al. (2012). A genome-wide association study identifies five loci influencing facial morphology in Europeans. PLoS Genet 8:e1002932. doi: 10.1371/journal.pgen.1002932
45. Manichaikul, A., Dupuis, J., Sen, S., and Broman, K. W. (2006). Poor performance of bootstrap confidence intervals for the location of a quantitative trait locus. Genetics 174, 481-489. doi: 10.1534/genetics.106.061549
46. Manichaikul, A., Moon, J. Y., Sen, S., Yandell, B. S., and Broman, K. W. (2009). A model selection approach for the identification of quantitative trait loci in experimental crosses, allowing epistasis. Genetics 181, 1077-1086. doi: 10.1534/genetics.108.094565
47. Mardia, K. V., Bookstein, F. L., and Moreton, I. J. (2000). Statistical assessment of bilateral symmetry of shapes. Biometrika 87, 285-300. doi: 10.1093/biomet/87.2.285
48. Nishimura, I., Drake, T. A., Lusis, A. J., Lyons, K. M., Nadeau, J. H., and Zernik, J. (2003). ENU Large-scale mutagenesis and quantitative trait linkage (QTL) analysis in mice: novel technologies for searching polygenetic determinants of craniofacial abnormalities. Crit. Rev. Oral Biol. Med . 14, 320-330. doi: 10.1177/154411130301400503
49. Norgard, E. A., Jarvis, J. P., Roseman, C. C., Maxwell, T. J., Kenney-Hunt, J. P., Samocha, K. E., et al. (2009). Replication of long-bone length QTL in the F9-F10 LG,SM advanced intercross. Mamm. Genome 20, 224-235. doi: 10.1007/s00335-009-9174-9
50. Olson, C. L. (1976). On choosing a test statistic in multivariate analysis of variance. Psychol. Bull . 83, 579-586. doi: 10.1037/0033-2909.83.4.579
51. Olson, C. L. (1979). Practical considerations in choosing a MANOVA test statistic: a rejoinder to Stevens. Psychol. Bull . 86, 1350-1352. doi: 10.1037/0033-2909.86.6.1350
52. Pallares, L. F., Harr, B., Turner, L. M., and Tautz, D. (2014). Use of a natural hybrid zone for genomewide association mapping of craniofacial traits in the house mouse. Mol. Ecol . 23, 5756-5770. doi: 10.1111/mec.12968
53. Pillai, K. C. S. (1967). Upper percentage points of the largest root of a matrix in multivariate analysis. Biometrika 54, 189. doi: 10.2307/2333862
54. Pohl, E., Aykut, A., Beleggia, F., Karaca, E., Durmaz, B., Keupp, K., et al. (2013). A hypofunctional PAX1 mutation causes autosomal recessively inherited otofaciocervical syndrome. Hum. Genet . 132, 1311-1320. doi: 10.1007/s00439-013-1337-9
55. Rainger, J., Bengani, H., Campbell, L., Anderson, E., Sokhi, K., Lam, W., et al. (2012). Miller (Genee-Wiedemann) syndrome represents a clinically and biochemically distinct subgroup of postaxial acrofacial dysostosis associated with partial deficiency of DHODH. Hum. Mol. Genet . 21, 3969-3983. doi: 10.1093/hmg/dds218
56. Richtsmeier, J. T., Deleon, V. B., and Lele, S. R. (2002). The promise of geometric morphometrics. Yearb. Phys. Anthropol . 45, 63-91. doi: 10.1002/ajpa.10174
57. Rohlf, F. J. (2000a). On the use of shape spaces to compare morphometric methods. Hystrix 11, 9-25. doi: 10.4404/hystrix-11.1-4134
58. Rohlf, F. J. (2000b). Statistical power comparisons among alternative morphometric methods. Am. J. Phys. Anthropol . 111, 463-478. doi: 10.1002/(SICI)1096-8644(200004)111:4<463::AID-AJPA3>3.0.CO;2-B
59. Rohlf, F. J. (2003). Bias and error in estimates of mean shape in geometric morphometrics. J. Hum. Evol . 44, 665-683. doi: 10.1016/S0047-2484(03)00047-2
60. Schlager, S. (2014). Morpho: Calculations and Visualisations Related to Geometric Morphometrics . Available online at: http://CRAN.R-project.org/package=3DMorpho.
61. Schoenebeck, J. J., Hutchinson, S. A., Byers, A., Beale, H. C., Carrington, B., Faden, D. L., et al. (2012). Variation of BMP3 contributes to dog breed skull diversity. PLoS Genet . 8: e1002849. doi: 10.1371/journal.pgen.1002849
62. Sen, S., and Churchill, G. A. (2001). A statistical framework for quantitative trait mapping. Genetics 159, 371-387.
63. Seto, M. L., Hing, A. V., Chang, J., Hu, M., Kapp-Simon, K. A., Patel, P. K., et al. (2007). Isolated sagittal and coronal craniosynostosis associated with TWIST box mutations. Am. J. Med. Genet. A . 143A, 678-686. doi: 10.1002/ajmg.a.31630
64. Sherwood, R. J., Duren, D. L., Havill, L. M., Rogers, J., Cox, L. A., Towne, B., et al. (2008). A genomewide linkage scan for quantitative trait loci influencing the craniofacial complex in baboons (Papio hamadryas spp.). Genetics 180, 619-628. doi: 10.1534/genetics.108.090407
65. Sherwood, R. J., Duren, D. L., Mahaney, M. C., Blangero, J., Dyer, T. D., Cole, S. A., et al. (2011). A genome-wide linkage scan for quantitative trait loci influencing the craniofacial complex in humans (Homo sapiens sapiens). Anat. Rec. Adv. Integr. Anat. Evol. Biol . 294, 664-675. doi: 10.1002/ar.21337
66. Sonnesen, L., Nolting, D., Kjaer, K. W., and Kjaer, I. (2008). Association between the development of the body axis and the craniofacial skeleton studied by immunohistochemical analyses using collagen II, Pax9, Pax1, and Noggin antibodies. Spine 33, 1622-1626. doi: 10.1097/BRS.0b013e31817b61d1
67. Suto, J.-I. (2009). Identification of multiple quantitative trait loci affecting the size and shape of the mandible in mice. Mamm. Genome Off. J. Int. Mamm. Genome Soc . 20, 1-13. doi: 10.1007/s00335-008-9154-5
68. Tabachnick, B. G., and Fidell, L. S. (2007). Using Multivariate Statistics, 5th Edn . Boston: Pearson.
69. Uz, E., Alanay, Y., Aktas, D., Vargel, I., Gucer, S., Tuncbilek, G., et al. (2010). Disruption of ALX1 causes extreme microphthalmia and severe facial clefting: expanding the spectrum of autosomal-recessive ALX-related frontonasal dysplasia. Am. J. Hum. Genet . 86, 789-796. doi: 10.1016/j.ajhg.2010.04.002
70. Vecchione, L., Miller, J., Byron, C., Cooper, G. M., Barbano, T., Cray, J., et al. (2010). Age-related changes in craniofacial morphology in GDF-8 (myostatin)-deficient mice. Anat. Rec. Hoboken N.J . 2007, 32-41. doi: 10.1002/ar.21024
71. Visel, A., Thaller, C., and Eichele, G. (2004). Genepaint.org: an atlas of gene expression patterns in the mouse embryo. Nucleic Acids Res . 32, D552-D556. doi: 10.1093/nar/gkh029
72. Walsh, D. M., Shalev, S. A., Simpson, M. A., Morgan, N. V., Gelman-Kohan, Z., Chemke, J., et al. (2013). Acrocallosal syndrome: Identification of a novel KIF7 mutation and evidence for oligogenic inheritance. Eur. J. Med. Genet . 56, 39-42. doi: 10.1016/j.ejmg.2012.10.004
73. Wolf, J. B., Leamy, L. J., Routman, E. J., and Cheverud, J. M. (2005). Epistatic pleiotropy and the genetic architecture of covariation within early and late-developing skull trait complexes in mice. Genetics 171, 683-694. doi: 10.1534/genetics.104.038885
74. Wolf, J. B., and Wade, M. J. (2009). What are maternal effects (and what are they not)? Philos. Trans. R. Soc. Lond. B Biol. Sci . 364, 1107-1115. doi: 10.1098/rstb.2008.0238
75. Workman, M. S., Leamy, L. J., Routman, E. J., and Cheverud, J. M. (2002). Analysis of quantitative trait locus effects on the size and shape of mandibular molars in mice. Genetics 160, 1573-1586.