Epistasis: Too often neglected in complex trait studies?

Nature Reviews Genetics

Volumn 5, Issue 8, 2004, Pages 618-625

  Carlborg, Örjan ^a   Haley, Chris S ^b  

^a UPPSALA UNIVERSITY   (Sweden)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL MODEL; COMPLEX TRAIT; DISEASE PREDISPOSITION; EPISTASIS; GENE INTERACTION; GENETIC TRAIT; GENETIC VARIABILITY; GENOTYPE ENVIRONMENT INTERACTION; HUMAN; NATURAL POPULATION; NONHUMAN; POPULATION GENETICS; POPULATION SIZE; PRIORITY JOURNAL; QUANTITATIVE TRAIT LOCUS; REVIEW; STATISTICAL ANALYSIS; STATISTICAL POWER;

ALLELES; ANIMALS; CHROMOSOME MAPPING; EPISTASIS, GENETIC; GENE FREQUENCY; GENES, DOMINANT; GENETICS, POPULATION; HUMANS; LINKAGE DISEQUILIBRIUM; MODELS, GENETIC; QUANTITATIVE TRAIT LOCI; QUANTITATIVE TRAIT, HERITABLE; VARIATION (GENETICS);

ANIMALIA;

EID: 3442894519     PISSN: 14710056     EISSN: None     Source Type: Journal    
DOI: 10.1038/nrg1407     Document Type: Review

References (71)

1. Phillips P. C. The language of gene interaction. Genetics 149, 1167-1171 (1998).
2. Hummel, K. P. The inheritance and expression of Disorganization, an unusual mutation in the mouse. J. Exp. Zool. 137, 389-423 (1958).
3. Tiret, L. et al. Synergistic effects of angiotensin-converting enzyme and angiotensin-II type 1 receptor gene polymorphisms on risk of myocardial infarction. Lancet 344, 910-913 (1994).
4. Flint, J. & Mott, R. Finding the molecular basis of quantitative traits: successes and pitfalls. Nature Rev. Genet. 2, 437-445 (2001).
5. Barton, N. H. & Keightley, P. D. Understanding quantitative genetic variation. Nature Rev. Genet. 3, 11-21 (2002).
6. Doerge, R. W. Mapping and analysis of quantitative trait loci in experimental populations. Nature Rev. Genet. 3, 43-52 (2002).
7. Jansen, R. C. Studying complex biological systems using multifactorial perturbation. Nature Rev. Genet. 4, 145-151 (2003).
8. Hoh, J. & Ott, J. Mathematical multi-locus approaches to localizing complex human trait genes. Nature Rev. Genet. 4, 701-709 (2003).
9. Hirschhorn, J. N., Lohmueller, K., Byrne, E. & Hirschhorn, K. A comprehensive review of genetic association studies. Genet Med. 4, 45-61 (2002).
10. Lander, E. S. & Botstein, D. Mapping Mendelian factors underlying quantitative traits using RFLP linkage maps. Genetics 121, 185-199 (1989).
11. Haseman, J. K. & Elston, R. C. The investigation of linkage between a quantitative trait and a marker locus. Behav. Genet. 2, 3-19 (1972).
12. Andersson, L. & Georges, M. Domestic-animal genomics: deciphering the genetics of complex traits. Nature Rev. Genet. 5, 202-212 (2004).
13. Mackay, T. F. Quantitative trait loci in Drosophila. Nature Rev. Genet. 1, 11-20 (2001).
14. Grobet, L. et al. A deletion in the bovine myostatin gene causes the double-muscled phenotype in cattle. Nature Genet. 17, 71-74 (1997).
15. van Laere, A. S. et al. A regulatory mutation in /GF2 causes a major QTL effect on muscle growth in the pig. Nature 425, 832-836 (2003).
16. Fjneman, R. J., de Vries, S. S., Jansen, R. C. & Demant, P. Complex interactions of new quantitative trait loci, Sluc1, Sluc2, Sluc3, and Sluc4, that influence the susceptibility to lung cancer in the mouse. Nature Genet. 14, 465-467 (1996).
17. Long, A. D., Mullaney, S. L., Mackay, T. F. & Langley, C. H. Genetic interactions between naturally occurring alleles at quantitative trait loci and mutant alleles at candidate loci affecting bristle number in Drosophila melanogaster. Genetics 144, 1497-1510 (1996).
18. Li, Z., Pinson, S. R., Park, W. D., Paterson, A. H. & Stansel, J. W. Epistasis for three grain yield components in rice (Oryza sativa L). Genetics 145, 453-465 (1997).
19. Shook, D, R. & Johnson, T. E. Quantitative trait loci affecting survival and fertility-related traits in Caenorhabditis elegans show genotype-environment interactions, pleiotropy and epistasis. Genetics 153, 1233-1243 (1999).
20. Morel, L. et al. Genetic reconstitution of systemic lupus erythematosus immunopathology with polycongenic murine strains. Proc. Natl Acad. Sci. USA 97, 6670-6675 (2000).
21. Stern M. P. et al. Evidence for linkage of regions on chromosomes 6 and 11 to plasma glucose concentrations in Mexican Americans. Genome Res. 6, 724-734 (1996).
22. Kao, C.-H., Zeng, Z.-B. & Teasdale, R. Multiple interval mapping for quantitative trait loci. Genetics 152, 1203-1216 (1999).
23. Sen, S. & Churchill, G. A. A statistical framework for quantitative trait mapping. Genetics 159, 371-387 (2001).
24. Carlborg, Ö. & Andersson, L. The use of randomisation testing for detection of multiple epistatic QTL. Genet. Res. 79, 175-184 (2002).
25. Yi, N., Xu, S. & Allison, D. B. Bayesian model choice and search strategies for mapping interacting quantitative trait loci. Genetics 165, 867-883 (2003).
26. Carlborg, Ö. et al. A global search reveals epistatic interaction between QTLs for early growth in the chicken. Genome Res. 13, 413-421 (2003).
27. Carlborg, Ö., Burt, D., Hocking, P. & Haley, C. S. Simultaneous mapping of epistatic QTL in chickens reveals clusters of QTL pairs with similar genetic effects on growth. Genet. Res (in the press).
28. Kim, J. H. et al. Genetic analysis of a new mouse model for non-insulin-dependent diabetes. Genomics 74, 273-286 (2001).
29. Shimomura, K. et al. Genome-wide epistatic interaction analysis reveals complex genetic determinants of circadian behavior in mice. Genome Res. 11, 959-980 (2001).
30. Sugiyama, F. et al. Concordance of murine quantitative trait loci for salt-induced hypertension with rat and human loci. Genomics 71, 70-77 (2001)
31. Peripato, A. C. et al. Quantitative trait loci for maternal performance for offspring survival in mice. Genetics 162, 1341-1353 (2002).
32. Ways, J. A., Cicila, G. T., Garrett, M. R. & Koch, L. G. A genome scan for loci associated with aerobic running capacity in rats. Genomics 80, 13-20 (2002).
33. Montooth, K. L., Marden, J. H. & Clark, A. G. Mapping determinants of variation in energy metabolism, respiration and fight in Drosophila. Genetics 165, 623-635 (2003).
34. Eshed, Y. & Zamir, D. Less-than-additive epistatic interactions of quantitative trait loci in tomato. Genetics 143, 1807-1817 (1996).
35. Flint, J., DeFries, J. C. & Henderson, N. D. Little epistasis for anxiety-related measures in the DeFries strains of laboratory mice. Mamm. Genome 15, 77-82 (2004).
36. Smith Richards, B. K. et al. QTL analysis of self-selected macronutrient diet intake: fat, carbohydrate, and total kilocalories. Physiol. Genomics 11, 205-217.
37. Zeng, Z-.B. et al. Genetic architecture of a morphological shape difference between two Drosophila species. Genetics 154, 299-310 (2000).
38. Beavis, W. D. in Molecular Dissection of Complex Traits (ed. Paterson, A. H.) 145-162 (CRC, New York, 1998).
39. Cordell, H. J. et al. Statistical modeling of interlocus interactions in a complex disease: rejection of the multiplicative model of epistasis in type 1 diabetes. Genetics 158, 357-367 (2001).
40. Risch, N., Ghosh, S. & Todd, J. A. Statistical evaluation of multiple-locus linkage data in experimental species and its relevance to human studies: application to nonobese diabetic (NOD) mouse and human insulin-dependent diabetes mellitus (IDDM). Am. J. Hum. Genet. 53, 702-714 (1993).
41. Cheverud, J. M. et al. Genetic architecture of adiposity in the cross of LG/J and SM/J inbred mice. Mamm. Genome 12, 3-12 (2001).
42. Omholt, S. W., Plante, E., Oyehaug, L. & Xiang, K. Gene regulatory networks generating the phenomena of additivity, dominance and epistasis. Genetics 155, 969-980 (2000).
43. Walling, G. A. et al. Combined analyses of data from QTL mapping studies: chromosome 4 effects on porcine growth and fatness. Genetics 155, 1369-1378 (2000).
44. Cordell, H. J., Todd, J. A., Bennett, S. T., Kawaguchi, Y. & Farrall, M. Two-locus maximum lod score analysis of a multifactorial trait: joint consideration of IDDM2 and IDDM4 with IDDM1 in type 1 diabetes. Am. J. Hum. Genet. 57, 920-934 (1995).
45. Cox, N. J. et al. Loci on chromosomes 2 (NIDDM1) and 15 interact to increase susceptibility to diabetes in Mexican Americans. Nature Genet. 21, 213-215 (1999).
46. Cho, J. H. et al. Identification of novel susceptibility loci for inflammatory bowel disease on chromosomes 1p, 3q, and 4q: evidence for epistasis between 1p and IBD1. Proc. Natl Acad. Sci. USA 95, 7502-7507 (1998).
47. The International HapMap Consortium. The International HapMap Project. Nature 426, 789-796 (2003).
48. Van Den Oord, E. J. & Neale, B. M. Will haplotype maps be useful for finding genes? Mol. Psychiatry 9, 227-236 (2004).
49. Blangero, J. & Almasy, L. Multipoint oligogenic linkage analysis of quantitative traits. Genet. Epidemiol. 14, 959-964 (1997).
50. Eaves, L. J. Effect of genetic architecture on the power of human linkage studies to resolve the contribution of quantitative trait loci. Heredity 72, 175-192 (1994).
51. Mitchell, B. D., Ghosh, S., Schneider, J. L., Birznieks, G. & Blangero, J. Power of variance component linkage analysis to detect epistasis. Genet. Epidemiol. 14, 1017-1022 (1997).
52. van den Oord, E. J. & Sullivan, P. F. False discoveries and models for gene discovery. Trends Genet. 19, 537-542 (2003).
53. Benjamini, Y. & Hochberg, Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. 57, 289-300 (1995).
54. Drawid, A. & Gerstein M. A Bayesian system integrating expression data with sequence patterns for localizing proteins: comprehensive application to the yeast genome. J. Mol. Biol. 301, 1059-1075 (2000).
55. Jenssen, T. K., Laegreid, A., Komorowski, J. & Hovig, E. A literature network of human genes for high-throughput analysis of gene expression. Nature Genet. 28, 21-28 (2001).
56. Andersson, L. Genetic dissection of phenotypic diversity in farm animals. Nature Rev. Genet. 2, 130-138 (2001).
57. Kijas, J. M. et al. Melanocortin receptor 1 (MC1R) mutations and coat color in pigs. Genetics 150, 1177-1185 (1998).
58. Haley, C. S. & Knott, S. A. A simple regression method for mapping quantitative trait loci in line crosses using flanking markers. Heredity 69, 315-324 (1992).
59. Cheverud, J. M. & Routman, E. J. Epistasis and its contribution to genetic variance components. Genetics 139, 1455-1461 (1995).
60. Chase, K., Adler, F. R. & Lark, K. G. Epistat: a computer program for identifying and testing interactions between pairs of quantitative trait loci. Theor. Appl. Genet. 94, 724-730 (1997).
61. Schaid, D. J. General score tests for associations of genetic markers with disease using cases and their parents Genet. Epidemiol. 13, 423-449 (1996).
62. Umbach, D. M. & Weinberg, C. R. Designing and analysing case-control studies to exploit independence of genotype and exposure. Stat. Med. 16, 1731-1743 (1997).
63. Rabinowitz, D. A transmission disequilibrium test for quantitative trait loci. Hum. Hered. 47, 342-350 (1997).
64. Almasy, L. & Biangero, J. Multipoint quantitative-trait linkage analysis in general pedigrees. Am. J. Hum. Genet. 62, 1198-1211 (1998).
65. George, V., Tiwari, H. K., Shu, Y, Zhu, X. & Elston, R. C. Linkage and association analyses of alcoholism using a regression-based transmission/disequilibrium test. Genet. Epidemiol. 17 (Suppl. 1), S157-S161 (1999).
66. Lunetta, K. L., Faraone, S. V., Biederman, J. & Laird, N. M. Family-based tests of association and linkage that use unaffected sibs, covariates, and interactions. Am. J. Hum. Genet. 66, 605-614 (2000).
67. Liu, Y., Tritchler, D. & Bull, S. B. A unified framework for transmission-disequilibrium test analysis of discrete and continuous traits Genet. Epidemiol. 22, 26-40 (2002).
68. Carlborg, Ö., Andersson, L. & Kinghorn, B. The use of a genetic algorithm for simultaneous mapping of multiple interacting quantitative trait loci. Genetics 155, 2003-2010 (2000).
69. Ljungberg, K., Holmgren, S. & Carlborg, Ö. Efficient algorithms for quantitative trait loci mapping problems. J. Comput. Biol. 9, 793-804 (2002).
70. Ljungberg, K., Holmgren, S. & Carlborg Ö. Simultaneous search for multiple QTL using the global optimization algorithm DIRECT. Bioinformatics 25 Mar 2004 (doi:10.1093/bioinformatics/bth175).
71. Churchill, G. A. & Doerge, R. W. Empirical threshold values for quantitative trait mapping. Genetics 138, 963-971 (1994).