High-Resolution genetic mapping of complex traits from a combined analysis of F2 and advanced intercross mice

Genetics

Volumn 198, Issue 1, 2014, Pages 103-116

  Parker, Clarissa C ^a   Carbonetto, Peter ^a,b   Sokoloff, Greta ^b   Park, Yeonhee J ^b   Abney, Mark ^b   Palmer, Abraham A ^b,c  

^a MIDDLEBURY COLLEGE   (United States)

^b THE UNIVERSITY OF CHICAGO   (United States)

^c Division of Biological Sciences and the Pritzker School of Medicine   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADVANCED INTERCROSS LINE; ANIMAL EXPERIMENT; ARTICLE; CHROMOSOME 17; CHROMOSOME 2; CHROMOSOME 4; CONTROLLED STUDY; DNA EXTRACTION; FEAR; FEMALE; GENE SEQUENCE; GENETIC ASSOCIATION; GENETIC DISTANCE; GENETIC LINKAGE; GENETIC MARKER; GENETIC RECOMBINATION; GENETIC VARIABILITY; GENOTYPE; HAPLOTYPE; HETEROZYGOTE; HOMOZYGOTE; INBRED MOUSE STRAIN; INBRED STRAIN; MALE; MOUSE; NONHUMAN; OPEN FIELD BEHAVIOR; PEDIGREE; PHENOTYPE; QUANTITATIVE TRAIT; QUANTITATIVE TRAIT LOCUS; QUANTITATIVE TRAIT LOCUS MAPPING; SINGLE NUCLEOTIDE POLYMORPHISM; X CHROMOSOME; ANIMAL; ANXIETY; CHROMOSOME; CHROMOSOME MAP; CONDITIONED REFLEX; GENETICS; HYBRIDIZATION;

ANIMALS; ANXIETY; CHROMOSOME MAPPING; CHROMOSOMES; CONDITIONING, CLASSICAL; FEAR; FEMALE; HYBRIDIZATION, GENETIC; MALE; MICE; MICE, INBRED STRAINS; PEDIGREE; POLYMORPHISM, SINGLE NUCLEOTIDE; QUANTITATIVE TRAIT LOCI;

EID: 84907965193     PISSN: 00166731     EISSN: 19432631     Source Type: Journal    
DOI: 10.1534/genetics.114.167056     Document Type: Article

References (79)

1. Abney, M., M. S. McPeek, and C. Ober, 2000 Estimation of variance components of quantitative traits in inbred populations. Am. J. Hum. Genet. 66: 629–650.
2. Abney, M., C. Ober, and M. S. McPeek, 2002 Quantitative-trait homozygosity and association mapping and empirical genomewide significance in large, complex pedigrees: fasting seruminsulin level in the Hutterites. Am. J. Hum. Genet. 70: 920–934.
3. Aulchenko, Y. S., D.-J. de Koning, and C. Haley, 2007 Genomewide rapid association using mixed model and regression: a fast and simple method for genomewide pedigree-based quantitative trait loci association analysis. Genetics 177: 577–585.
4. Bartnikas, T. B., C. C. Parker, R. Cheng, D.R. Campagna, J. E. Lim, et al., 2012 QTLs for murine red blood cell parameters in LG/J and SM/ J F2 and advanced intercross lines. Mamm. Genome 23: 356–366.
5. Broman, K. W., 2012 Haplotype probabilities in advanced intercross populations. G3 2: 199-202.
6. Broman, K. W., and S. Sen, 2009 A Guide to QTL Mapping with R-qtl. Springer-Verlag, Berlin/Heidelberg, Germany/New York.
7. Bryant, C. D., C. C. Parker, L. Zhou, C. Olker, R. Y. Chandrasekaran et al., 2012 Csnk1e is a genetic regulator of sensitivity to psychostimulants and opioids. Neuropsychopharmacology 37: 1026–1035.
8. Caldarone, B., C. Saavedra, K. Tartaglia, J. M. Wehner et al., 1997 Quantitative trait loci analysis affecting contextual conditioning in mice. Nat. Genet 17: 335–337.
9. Cheng, R., and A. A. Palmer, 2013 A simulation study of permutation, bootstrap, and gene dropping for assessing statistical significance in the case of unequal relatedness. Genetics 193: 1015–1018.
10. Cheng, R., J. E. Lim, K. E. Samocha, G. Sokoloff, M. Abney et al., 2010 Genome-wide association studies and the problem of relatedness among advanced intercross lines and other highly recombinant populations. Genetics 185: 1033–1044.
11. Cheng, R., M. Abney, A. A. Palmer, and A. D. Skol, 2011 QTLRel: an R package for genome-wide association studies in which relatedness is a concern. BMC Genet. 12: 66.
12. Cheng, R., C. C. Parker, M. Abney, and A. A. Palmer, 2013 Practical considerations regarding the use of genotype and pedigree data to model relatedness in the context of genome-wide association studies. G3 3: 1861–1867.
13. Churchill, G. A., and R. W. Doerge, 1994 Empirical threshold values for quantitative trait mapping. Genetics 138: 963–971.
14. Cox, A., C. L. Ackert-Bicknell, B. L. Dumont, Y. Ding, J. T. Bell et al., 2009 A new standard genetic map for the laboratory mouse. Genetics 182: 1335–1344.
15. Darvasi, A., and M. Soller, 1995 Advanced intercross lines, an experimental population for fine genetic mapping. Genetics 141: 1199–1207.
16. Demyttenaere, K., R. Bruffaerts, J. Posada-Villa, I. Gasquet, V. Kovess et al., 2004 Prevalence, severity, and unmet need for treatment of mental disorders in the World Health Organization World Mental Health Surveys. JAMA 291: 2581–2590.
17. Donner, J., S. Pirkola, K. Silander, L. Kananen, J. D. Terwilliger et al., 2008 An association analysis of murine anxiety genes in humans implicates novel candidate genes for anxiety disorders. Biol. Psychiatry 64: 672–680.
18. Fanselow, M. S., and J. E. LeDoux, 1999 Why we think plasticity underlying Pavlovian fear conditioning occurs in the basolateral amygdala. Neuron 23: 229–232.
19. Flint, J., 2011 Mapping quantitative traits and strategies to find quantitative trait genes. Methods 53: 163–174.
20. Flint, J., and E. Eskin, 2012 Genome-wide association studies in mice. Nat. Rev. Genet. 13: 807–817.
21. Flint, J., and S. Shifman, 2008 Animal models of psychiatric disease. Curr. Opin. Genet. Dev. 18: 235–240.
22. Hettema, J. M., B. T. Webb, A.-Y. Guo, Z. Zhao, B. S. Maher et al., 2011 Prioritization and association analysis of murine-derived candidate genes in anxiety-spectrum disorders. Biol. Psychiatry 70: 888–896.
23. Heydendael, W., A. Sengupta, S. Beck, and S. Bhatnagar, 2013 Optogenetic examination identifies a context-specific role for orexins/hypocretins in anxiety-related behavior. Physiol. Behav. 130: 182–190.
24. Hovatta, I., and C. Barlow, 2008 Molecular genetics of anxiety in mice and men. Ann. Med. 40: 92–109.
25. Hovatta, I., R. S. Tennant, R. Helton, R. A. Marr, O. Singer et al., 2005 Glyoxalase 1 and glutathione reductase 1 regulate anxiety in mice. Nature 438: 662–666.
26. Jackson, I. J., 1994 Molecular and developmental genetics of mouse coat color. Annu. Rev. Genet. 28: 189–217.
27. Jackson, I. J., 1997 Homologous pigmentation mutations in human, mouse and othermodel organisms. Hum. Mol. Genet. 6: 1613–1624.
28. Jones, B.C., L. M. Tarantino, L. A. Rodriguez, C. L. Reed, G. E. McClearn et al., 1999 Quantitative-trait loci analysis of cocaine-related behaviors and neurochemistry. Pharmacogenetics 9: 607–17.
29. Jovanovic, T., and K. J. Ressler, 2010 How the neurocircuitry and genetics of fear inhibition may inform our understanding of PTSD. Am. J. Psychiatry 167: 648–662.
30. Kalueff, A. V., M. Wheaton, and D. L. Murphy, 2007 What’s wrong with my mouse model? Advances and strategies in animal modeling of anxiety and depression. Behav. Brain Res. 179: 1–18.
31. Kang, H. M., N. A. Zaitlen, C. M. Wade, A. Kirby, D. Heckerman et al., 2008 Efficient control of population structure in model organism association mapping. Genetics 178: 1709–1723.
32. Kang, H. M., J. H. Sul, S. K. Service, N. A. Zaitlen, S.-Y. Kong et al., 2010 Variance component model to account for sample structure in genome-wide association studies. Nat. Genet. 42: 348–354.
33. Karigl, G., 1981 A recursive algorithm for the calculation of identity coefficients. Ann. Hum. Genet. 45: 299–305.
34. Kessler, R. C., P. Berglund, O. Demler, R. Jin, K. R. Merikangas et al., 2005a Lifetime prevalence and age-of-onset distributions of DSM-IV disorders in the National Comorbidity Survey Replication. Arch. Gen. Psychiatry 62: 593–602.
35. Kessler, R. C., W. T. Chiu, O. Demler, K. R. Merikangas, and E. E. Walters, 2005b Prevalence, severity, and comorbidity of 12- month DSM-IV disorders in the National Comorbidity Survey Replication. Arch. Gen. Psychiatry 62: 617–627.
36. Lander, E. S., and P. Green, 1987 Construction of multilocus genetic linkage maps in humans. Proc. Natl. Acad. Sci. USA 84: 2363–2367.
37. Lange, K., 2002 Mathematical and Statistical Methods for Genetic Analysis. Springer-Verlag, Berlin/Heidelberg, Germany/New York.
38. Legare, M. E., F. S. Bartlett, and W. N. Frankel, 2000 A major effect QTL determined by multiple genes in epileptic EL mice. Genome Res. 10: 42–48.
39. Lionikas, A., R. Cheng, J. E. Lim, A. A. Palmer, and D. A. Blizard, 2010 Fine-mapping of muscle weight QTL in LG/J and SM/J intercrosses. Physiol. Genomics 42A: 33–38.
40. Lippert, C., J. Listgarten, Y. Liu, C. M. Kadie, R. I. Davidson et al., 2011 FaST linear mixed models for genome-wide association studies. Nat. Methods 8: 833–835.
41. Listgarten, J., C. Lippert, C. M. Kadie, R. I. Davidson, E. Eskin et al., 2012 Improved linear mixed models for genome-wide association studies. Nat. Methods 9: 525–526.
42. López-Aumatell, R., E. Vicens-Costa, M. Guitart-Masip, E. Martínez-Membrives, W. Valdar et al., 2009 Unlearned anxiety predicts learned fear: a comparison among heterogeneous rats and the Roman rat strains. Behav. Brain Res. 202: 92–101.
43. Mahan, A. L., and K. J. Ressler, 2012 Fear conditioning, synaptic plasticity and the amygdala: implications for posttraumatic stress disorder. Trends Neurosci. 35: 24–35.
44. Manichaikul, A., J. Dupuis, S. Sen, and K. W. Broman, 2006 Poor performance of bootstrap confidence intervals for the location of a quantitative trait locus. Genetics 174: 481–489.
45. Mott, R., C. J. Talbot, M. G. Turri, A. C. Collins, and J. Flint, 2000 A method for fine mapping quantitative trait loci in outbred animal stocks. Proc. Natl. Acad. Sci. USA 97: 12649–12654.
46. Nakamura, K., Y. Xiu, M. Ohtsuji, G. Sugita, M. Abe et al., 2003 Genetic dissection of anxiety in autoimmune disease. Hum. Mol. Genet. 12: 1079–86.
47. Nicolae, D. L., E. Gamazon, W. Zhang, S. Duan, M. E. Dolan et al., 2010 Trait-associated SNPs are more likely to be eQTLs: annotation to enhance discovery from GWAS. PLoS Genet. 6: e1000888.
48. Norgard, E. A., H. A. Lawson, L. S. Pletscher, B. Wang, V. R. Brooks et al., 2011 Genetic factors and diet affect long-bone length in the F34 LG,SM advanced intercross. Mamm. Genome 22: 178–196.
49. Palmer, A. A., M. Verbitsky, R. Suresh, H.M. Kamens, C. L. Reed et al., 2005 Gene expression differences in mice divergently selected for methamphetamine sensitivity. Mamm. Genome 16: 291–305.
50. Pan, L., C. Ober, and M. Abney, 2007 Heritability estimation of sex-specific effects on human quantitative traits. Genet. Epidemiol. 31: 338–347.
51. Parker, C. C., and A. A. Palmer, 2011 Dark matter: Are mice the solution to missing heritability? Front. Genet. 2: 32.
52. Parker, C. C., R. Cheng, G. Sokoloff, J. E. Lim, A. D. Skol et al., 2011 Fine-mapping alleles for body weight in LG/J 3 SM/J F2 and F34 advanced intercross lines. Mamm. Genome 22: 563–571.
53. Parker, C. C., R. Cheng, G. Sokoloff, and A. A. Palmer, 2012a Genomewide association for methamphetamine sensitivity in an advanced intercross mouse line. Genes Brain Behav. 11: 52–61.
54. Parker, C. C., G. Sokoloff, R. Cheng, and A. A. Palmer, 2012b Genomewide association for fear conditioning in an advanced intercross mouse line. Behav. Genet. 42: 437–448.
55. Parker, C. C., G. Sokoloff, E. Leung, S. L. Kirkpatrick, and A. A. Palmer, 2013 A large QTL for fear and anxiety mapped using an F2 cross can be dissected into multiple smaller QTLs. Genes Brain Behav. 12: 714–722.
56. Petkov, P. M., Y. Ding, M. A. Cassell, W. Zhang, G. Wagner et al., 2004 An efficient SNP system for mouse genome scanning and elucidating strain relationships. Genome Res. 14: 1806–1811.
57. Ponder, C. A., C. L. Kliethermes, M. R. Drew, J. Muller, K. Das et al., 2007a Selection for contextual fear conditioning affects anxietylike behaviors and gene expression. Genes Brain Behav. 6: 736–749.
58. Ponder, C. A., M. Munoz, T. C. Gilliam, and A. A. Palmer, 2007b Genetic architecture of fear conditioning in chromosome substitution strains: relationship to measures of innate (unlearned) anxiety-like behavior. Mamm. Genome 18: 221–228.
59. Radcliffe, R. A., M. V. Lowe, and J. M. Wehner, 2000 Confirmation of contextual fear conditioning QTLs by short-term selection. Behav. Genet. 30: 183–191.
60. Samocha, K. E., J. E. Lim, R. Cheng, G. Sokoloff, and A. A. Palmer, 2010 Fine mapping of QTL for prepulse inhibition in LG/J and SM/J mice using F2 and advanced intercross lines. Genes Brain Behav. 9: 759–767.
61. Schaub, M. A., A. P. Boyle, A. Kundaje, S. Batzoglou, and M. Snyder, 2012 Linking disease associations with regulatory information in the human genome. Genome Res. 22: 1748–1759.
62. Schwander, M., W. Xiong, J. Tokita, A. Lelli, H. M. Elledge et al., 2009 A mouse model for nonsyndromic deafness (DFNB12) links hearing loss to defects in tip links of mechanosensory hair cells. Proc. Natl. Acad. Sci. USA 106: 5252–5257.
63. Shao, H., D. S. Sinasac, L. C. Burrage, C. A. Hodges, P. J. Supelak et al., 2010 Analyzing complex traits with congenic strains. Mamm. Genome 21: 276–286.
64. Sherry, S. T., M. H. Ward, M. Kholodov, J. Baker, L. Phan et al., 2001 dbSNP: the NCBI database of genetic variation. Nucleic Acids Res. 29: 308–311.
65. Shmelkov, S. V., A. Hormigo, D. Jing, C. C. Proenca, K. G. Bath et al., 2010 Slitrk5 deficiency impairs corticostriatal circuitry and leads to obsessive-compulsive-like behaviors in mice. Nat. Med. 16: 598–602.
66. Sokoloff, G., C. C. Parker, J. E. Lim, and A. A. Palmer, 2011 Anxiety and fear in a cross of C57BL/6J and DBA/2J mice: mapping overlapping and independent QTL for related traits. Genes Brain Behav. 10: 604–614.
67. Stephens, M., 2013 A unified framework for association analysis with multiple related phenotypes. PLoS ONE 8: e65245.
68. Sullivan, P. F., M. J. Daly, and M. O’Donovan, 2012 Genetic architectures of psychiatric disorders: the emerging picture and its implications. Nat. Rev. Genet. 13: 537–551.
69. Sun, L., H. L. Gooding, P. J. Brunton, J. A. Russell, R. Mitchell et al., 2013 Phospholipase D-mediated hypersensitivity at central synapses is associated with abnormal behaviours and pain sensitivity in rats exposed to prenatal stress. Int. J. Biochem. Cell Biol. 45: 2706–2712.
70. Talbot, C. J., R. A. Radcliffe, J. Fullerton, R. Hitzemann, J. M. Wehner et al., 2003 Fine scale mapping of a genetic locus for conditioned fear. Mamm. Genome 14: 223–230.
71. Terracciano, A., S. Sanna, M. Uda, B. Deiana, G. Usala et al., 2010 Genome-wide association scan for five major dimensions of personality. Mol. Psychiatry 15: 647–656.
72. Thifault, S., S. Ondrej, Y. Sun, A. Fortin, E. Skamene et al., 2008 Genetic determinants of emotionality and stress response in AcB/BcA recombinant congenic mice and in silico evidence of convergence with cardiovascular candidate genes. Hum. Mol. Genet. 17: 331–44.
73. Wilson, Y. M., T. C. Brodnicki, A. J. Lawrence, and M. Murphy, 2011 Congenic mouse strains enable discrimination of genetic determinants contributing to fear and fear memory. Behav. Genet. 41: 278–287.
74. Wise, A. L., L. Gyi, and T. A. Manolio, 2013 eXclusion: toward integrating the X chromosome in genome-wide association analyses. Am. J. Hum. Genet. 92: 643–647.
75. Yang, J., N. A. Zaitlen, M. E. Goddard, P. M. Visscher, and A. L. Price, 2014 Advantages and pitfalls in the application of mixed-model association methods. Nat. Genet. 46: 100–106.
76. Yu, J., G. Pressoir, W. H. Briggs, I. V. Bi, M. Yamasaki et al., 2006 A unified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nat. Genet. 38: 203–208.
77. Zhou, X., and M. Stephens, 2012 Genome-wide efficient mixedmodel analysis for association studies. Nat. Genet. 44: 821–824.
78. Zhou, X., P. Carbonetto, and M. Stephens, 2013 Polygenic modeling with Bayesian sparse linearmixedmodels. PLoS Genet. 9: e1003264.
79. Zou, F., J. A. L. Gelfond, D. C. Airey, L. Lu, K. F. Manly et al., 2005 Quantitative trait locus analysis using recombinant inbred intercrosses: theoretical and empirical considerations. Genetics 170: 1299–1311.