Genome-wide association of multiple complex traits in outbred mice by ultra-low-coverage sequencing

Nature Genetics

Volumn 48, Issue 8, 2016, Pages 912-918

  Nicod, Jérôme ^a   Davies, Robert W ^a   Cai, Na ^a   Hassett, Carl ^b   Goodstadt, Leo ^a   Cosgrove, Cormac ^c   Yee, Benjamin K ^d   Lionikaite, Vikte ^e   McIntyre, Rebecca E ^f   Remme, Carol Ann ^g   Lodder, Elisabeth M ^g   Gregory, Jennifer S ^e   Hough, Tertius ^b   Joynson, Russell ^b   Phelps, Hayley ^b   Nell, Barbara ^b   Rowe, Clare ^b   Wood, Joe ^b   Walling, Alison ^b   Bopp, Nasrin ^a   Bhomra, Amarjit ^a   Hernandez Pliego, Polinka ^a   Callebert, Jacques ^h   Aspden, Richard M ^e   Talbot, Nick P ⁱ   Robbins, Peter A ⁱ   Harrison, Mark ^b   Fray, Martin ^b   Launay, Jean Marie ^h   Pinto, Yigal M ^g   Blizard, David A ^j   Bezzina, Connie R ^g   Adams, David J ^f   Franken, Paul ^k   Weaver, Tom ^b   Wells, Sara ^b   Brown, Steve D M ^l   Potter, Paul K ^l   Klenerman, Paul ^c   Lionikas, Arimantas ^e   Mott, Richard ^a,m   Flint, Jonathan ^a,n   more..

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b Medical Research Council Harwell Institute   (United Kingdom)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d HONG KONG POLYTECHNIC UNIVERSITY   (Hong Kong)

^e UNIVERSITY OF ABERDEEN   (United Kingdom)

^f WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^g ACADEMIC MEDICAL CENTER   (Netherlands)

^h HÔPITAL LARIBOISIÈRE   (France)

ⁱ UNIVERSITY OF OXFORD   (United Kingdom)

^j PENNSYLVANIA STATE UNIVERSITY   (United States)

^k UNIVERSITY OF LAUSANNE   (Switzerland)

^l MRC MAMMALIAN GENETICS UNIT   (United Kingdom)

^m UNIVERSITY COLLEGE LONDON   (United Kingdom)

ⁿ UNIVERSITY OF CALIFORNIA   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ANIMAL EXPERIMENT; ARTICLE; BONE MINERAL; FEMALE; GENE; GENE LOCUS; GENE SEQUENCE; GENOME-WIDE ASSOCIATION STUDY; HAPLOTYPE; MALE; MAMMAL; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; QUANTITATIVE TRAIT LOCUS; SLEEP; T LYMPHOCYTE; ULTRA LOW COVERAGE SEQUENCING; WOUND HEALING; ANIMAL; CHROMOSOMAL MAPPING; GENETIC MARKER; GENETICS; GENOTYPE; MULTIFACTORIAL INHERITANCE; OUTBRED STRAIN; SINGLE NUCLEOTIDE POLYMORPHISM;

GENETIC MARKER;

ANIMALS; ANIMALS, OUTBRED STRAINS; CHROMOSOME MAPPING; GENETIC MARKERS; GENOME-WIDE ASSOCIATION STUDY; GENOTYPE; HAPLOTYPES; MICE; MULTIFACTORIAL INHERITANCE; PHENOTYPE; POLYMORPHISM, SINGLE NUCLEOTIDE; QUANTITATIVE TRAIT LOCI;

EID: 84976878592     PISSN: 10614036     EISSN: 15461718     Source Type: Journal    
DOI: 10.1038/ng.3595     Document Type: Article

References (58)

1. Flint, J. &Eskin, E. Genome-wide association studies in mice. Nat. Rev. Genet. 13, 807-817 (2012)
2. Visscher, P.M., Brown, M.A., McCarthy, M.I. &Yang, J. Five years of GWAS discovery. Am. J. Hum. Genet. 90, 7-24 (2012)
3. Atwell, S. et al. Genome-wide association study of 107 phenotypes in Arabidopsis thaliana inbred lines. Nature 465, 627-631 (2010)
4. Huang, X. et al. Genome-wide association studies of 14 agronomic traits in rice landraces. Nat. Genet. 42, 961-967 (2010)
5. Yalcin, B. et al. Commercially available outbred mice for genome-wide association studies. PLoS Genet. 6, e1001085 (2010)
6. 1000 Genomes Project Consortium. A map of human genome variation from population-scale sequencing. Nature 467, 1061-1073 (2010)
7. Marchini, J. &Howie, B. Genotype imputation for genome-wide association studies. Nat. Rev. Genet. 11, 499-511 (2010)
8. McKenna, A. et al. The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 20, 1297-1303 (2010)
9. Davies, R.W., Flint, J., Myers, S. &Mott, R. Rapid genotype imputation from sequence without reference panels. Nat. Genet. http://dx.doi.org/10.1038/ng.3594 (2016)
10. Yang, H. et al. A customized and versatile high-density genotyping array for the mouse. Nat. Methods 6, 663-666 (2009)
11. Baud, A. et al. Combined sequence-based and genetic mapping analysis of complex traits in outbred rats. Nat. Genet. 45, 767-775 (2013)
12. Keane, T.M. et al. Mouse genomic variation and its effect on phenotypes and gene regulation. Nature 477, 289-294 (2011)
13. Bennett, B.J. et al. A high-resolution association mapping panel for the dissection of complex traits in mice. Genome Res. 20, 281-290 (2010)
14. Valdar, W. et al. Genome-wide genetic association of complex traits in heterogeneous stock mice. Nat. Genet. 38, 879-887 (2006)
15. Wong, K. et al. Sequencing and characterization of the FVB/NJ mouse genome. Genome Biol. 13, R72 (2012)
16. Listgarten, J. et al. Improved linear mixed models for genome-wide association studies. Nat. Methods 9, 525-526 (2012)
17. Yang, J., Zaitlen, N.A., Goddard, M.E., Visscher, P.M. &Price, A.L. Advantages and pitfalls in the application of mixed-model association methods. Nat. Genet. 46, 100-106 (2014)
18. Cheng, R., Parker, C.C., Abney, M. &Palmer, A.A. Practical considerations regarding the use of genotype and pedigree data to model relatedness in the context of genome-wide association studies. G3 (Bethesda) 3, 1861-1867 (2013)
19. Manichaikul, A., Dupuis, J., Sen, S. &Broman, K.W. Poor performance of bootstrap confidence intervals for the location of a quantitative trait locus. Genetics 174, 481-489 (2006)
20. Weng, W. &Breslow, J.L. Dramatically decreased high density lipoprotein cholesterol, increased remnant clearance, and insulin hypersensitivity in apolipoprotein A-II knockout mice suggest a complex role for apolipoprotein A-II in atherosclerosis susceptibility. Proc. Natl. Acad. Sci. USA 93, 14788-14794 (1996)
21. Coury, F. et al. SLC4A2-mediated Cl-/HCO3-exchange activity is essential for calpain-dependent regulation of the actin cytoskeleton in osteoclasts. Proc. Natl. Acad. Sci. USA 110, 2163-2168 (2013)
22. Bladt, F., Riethmacher, D., Isenmann, S., Aguzzi, A. &Birchmeier, C. Essential role for the c-met receptor in the migration of myogenic precursor cells into the limb bud. Nature 376, 768-771 (1995)
23. Dietrich, S. et al. The role of SF/HGF and c-Met in the development of skeletal muscle. Development 126, 1621-1629 (1999)
24. Webster, M.T. &Fan, C.M. c-MET regulates myoblast motility and myocyte fusion during adult skeletal muscle regeneration. PLoS One 8, e81757 (2013)
25. Zhang, X.K. et al. The transcription factor Fli-1 modulates marginal zone and follicular B cell development in mice. J. Immunol. 181, 1644-1654 (2008)
26. Cryan, J.F. et al. Antidepressant and anxiolytic-like effects in mice lacking the group III metabotropic glutamate receptor mGluR7. Eur. J. Neurosci. 17, 2409-2417 (2003)
27. Duprez, D.M., Coltey, M., Amthor, H., Brickell, P.M. &Tickle, C. Bone morphogenetic protein-2 (BMP-2) inhibits muscle development and promotes cartilage formation in chick limb bud cultures. Dev. Biol. 174, 448-452 (1996)
28. Dougherty, S.E. et al. Mice lacking the transcriptional coactivator PGC-1α exhibit alterations in inhibitory synaptic transmission in the motor cortex. Neuroscience 271, 137-148 (2014)
29. Nakura, A., Higuchi, C., Yoshida, K. &Yoshikawa, H. PKCα suppresses osteoblastic differentiation. Bone 48, 476-484 (2011)
30. Galea, G.L. et al. Protein kinase Cα (PKCα) regulates bone architecture and osteoblast activity. J. Biol. Chem. 289, 25509-25522 (2014)
31. Sanyal, M. et al. B-cell development fails in the absence of the Pbx1 proto-oncogene. Blood 109, 4191-4199 (2007)
32. Kennedy, M.K. et al. Reversible defects in natural killer and memory CD8 T cell lineages in interleukin 15-deficient mice. J. Exp. Med. 191, 771-780 (2000)
33. Cannarile, M.A. et al. Transcriptional regulator Id2 mediates CD8+ T cell immunity. Nat. Immunol. 7, 1317-1325 (2006)
34. Chen, Z., Cooper, B., Kalla, S., Varoqueaux, F. &Young, S.M. Jr. The Munc13 proteins differentially regulate readily releasable pool dynamics and calcium-dependent recovery at a central synapse. J. Neurosci. 33, 8336-8351 (2013)
35. Reddy, S.Y. et al. Sleep quality, BDNF genotype and gene expression in individuals with chronic abdominal pain. BMC Med. Genomics 7, 61 (2014)
36. Melcher, T. et al. RED2, a brain-specific member of the RNA-specific adenosine deaminase family. J. Biol. Chem. 271, 31795-31798 (1996)
37. Mittaz, L., Antonarakis, S.E., Higuchi, M. &Scott, H.S. Localization of a novel human RNA-editing deaminase (hRED2 or ADARB2) to chromosome 10p15. Hum. Genet. 100, 398-400 (1997)
38. Collier, F.M. et al. Identification and characterization of a lymphocytic Rho-GTPase effector: rhotekin-2. Biochem. Biophys. Res. Commun. 324, 1360-1369 (2004)
39. Ramos-Quiroga, J.A. et al. Genome-wide copy number variation analysis in adult attention-deficit and hyperactivity disorder. J. Psychiatr. Res. 49, 60-67 (2014)
40. Peirce, J.L., Lu, L., Gu, J., Silver, L.M. &Williams, R.W. A new set of BXD recombinant inbred lines from advanced intercross populations in mice. BMC Genet. 5, 7 (2004)
41. Churchill, G.A. et al. The Collaborative Cross, a community resource for the genetic analysis of complex traits. Nat. Genet. 36, 1133-1137 (2004)
42. Svenson, K.L. et al. High-resolution genetic mapping using the Mouse Diversity outbred population. Genetics 190, 437-447 (2012)
43. Pallares, L.F. et al. Mapping of craniofacial traits in outbred mice identifies major developmental genes involved in shape determination. PLoS Genet. 11, e1005607 (2015)
44. Zaffaroni, D. et al. Met proto-oncogene juxtamembrane rare variations in mouse and humans: differential effects of Arg and Cys alleles on mouse lung tumorigenesis. Oncogene 24, 1084-1090 (2005)
45. Ma, P.C. et al. c-MET mutational analysis in small cell lung cancer: novel juxtamembrane domain mutations regulating cytoskeletal functions. Cancer Res. 63, 6272-6281 (2003)
46. Bloemberg, D. &Quadrilatero, J. Rapid determination of myosin heavy chain expression in rat, mouse, and human skeletal muscle using multicolor immunofluorescence analysis. PLoS One 7, e35273 (2012)
47. Varban, M.L. et al. Targeted mutation reveals a central role for SR-BI in hepatic selective uptake of high density lipoprotein cholesterol. Proc. Natl. Acad. Sci. USA 95, 4619-4624 (1998)
48. Muñoz-Bravo, J.L. et al. GDNF is required for neural colonization of the pancreas. Development 140, 3669-3679 (2013)
49. R Core Team. R: A Language and Environment for Statistical Computing 3.1.3 edn (R Foundation for Statistical Computing, 2015)
50. Lamble, S. et al. Improved workflows for high throughput library preparation using the transposome-based Nextera system. BMC Biotechnol. 13, 104 (2013)
51. Li, H. &Durbin, R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25, 1754-1760 (2009)
52. Lunter, G. &Goodson, M. Stampy: a statistical algorithm for sensitive and fast mapping of Illumina sequence reads. Genome Res. 21, 936-939 (2011)
53. Li, H. et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics 25, 2078-2079 (2009)
54. DePristo, M.A. et al. A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat. Genet. 43, 491-498 (2011)
55. Yalcin, B. et al. Sequence-based characterization of structural variation in the mouse genome. Nature 477, 326-329 (2011)
56. Li, N. &Stephens, M. Modeling linkage disequilibrium and identifying recombination hotspots using single-nucleotide polymorphism data. Genetics 165, 2213-2233 (2003)
57. Scheet, P. &Stephens, M. A fast and flexible statistical model for large-scale population genotype data: applications to inferring missing genotypes and haplotypic phase. Am. J. Hum. Genet. 78, 629-644 (2006)
58. 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)