Identification of epistatic effects using a protein-protein interaction database.

Epistasis (i.e. gene-gene interaction) has long been recognized as an important mechanism underlying the complexity of the genetic architecture of human traits. Definitions of epistasis range from the purely molecular to the traditional statistical measures of interaction. The statistical detection of epistasis usually does not map onto or easily relate to the biological interactions between genetic variations through their combined influence on gene expression or through their interactions at the gene product (i.e. protein) or DNA level. Recently, greater high-dimensional data on protein-protein interaction (PPI) and gene expression profiles have been collected that enumerates sets of biological interactions. To better align statistical and molecular models of epistasis, we present an example of how to incorporate the PPI information into the statistical analysis of interactions between copy number variations (CNVs). Among the 23 640 pairs of known human PPIs and the 1141 common CNVs detected among HapMap samples, we identified 37 pairs of CNVs overlapping with both genes of a PPI pair. Two CNV pairs provided sufficient genotype variation to search for epistatic effects on gene expression. Using 47 294 probe-specific gene expression levels as the outcomes, five epistatic effects were identified with P-value less than 10(-6). We found a CNV-CNV interaction significantly associated with gene expression of TP53TG3 (P-value of 2 × 10(-20)). The proteins associated with the CNV pair also bind TP53 which regulates the transcription of TP53TG3. This study demonstrates that using PPI data can assist in targeting statistical hypothesis testing to biological plausible epistatic interaction that reflects molecular mechanisms.

[1]  W. Bateson Mendel's Principles of Heredity , 1910, Nature.

[2]  R. Fisher XV.—The Correlation between Relatives on the Supposition of Mendelian Inheritance. , 1919, Transactions of the Royal Society of Edinburgh.

[3]  D. Ratner,et al.  Induction and modulation of cell-type-specific gene expression in dictyostelium , 1983, Cell.

[4]  S. Okamura,et al.  Isolation and characterization of a novel TP53‐inducible gene, TP53TG3 , 1999, Genes, chromosomes & cancer.

[5]  M. Wade,et al.  Epistasis and the Evolutionary Process , 2000 .

[6]  T. Ogihara,et al.  Association of a Sodium Channel α Subunit Promoter Variant with Blood Pressure , 2001 .

[7]  J. H. Moore,et al.  Multifactor-dimensionality reduction reveals high-order interactions among estrogen-metabolism genes in sporadic breast cancer. , 2001, American journal of human genetics.

[8]  K. Harvey,et al.  The Nedd4-like Protein KIAA0439 Is a Potential Regulator of the Epithelial Sodium Channel* , 2001, The Journal of Biological Chemistry.

[9]  R. Petersen,et al.  Corticobasal Degeneration and Frontotemporal Dementia Presentations in a Kindred with Nonspecific Histopathology , 2002, Dementia and Geriatric Cognitive Disorders.

[10]  Daniel R. Richards,et al.  Dissecting the architecture of a quantitative trait locus in yeast , 2002, Nature.

[11]  David Botstein,et al.  Systemic and cell type-specific gene expression patterns in scleroderma skin , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[12]  Toshihiro Tanaka The International HapMap Project , 2003, Nature.

[13]  Janel O. Johnson,et al.  α-Synuclein Locus Triplication Causes Parkinson's Disease , 2003, Science.

[14]  Gary D Bader,et al.  Global Mapping of the Yeast Genetic Interaction Network , 2004, Science.

[15]  Thomas Mitchell-Olds,et al.  Epistasis and balanced polymorphism influencing complex trait variation , 2005, Nature.

[16]  Ash A. Alizadeh,et al.  Cell-type specific gene expression profiles of leukocytes in human peripheral blood , 2006, BMC Genomics.

[17]  H. Lehrach,et al.  A Human Protein-Protein Interaction Network: A Resource for Annotating the Proteome , 2005, Cell.

[18]  Dmitrij Frishman,et al.  The MIPS mammalian protein?Cprotein interaction database , 2005, Bioinform..

[19]  T. Mackay,et al.  Of flies and man: Drosophila as a model for human complex traits. , 2006, Annual review of genomics and human genetics.

[20]  D. Reich,et al.  Principal components analysis corrects for stratification in genome-wide association studies , 2006, Nature Genetics.

[21]  Sean R. Collins,et al.  Global landscape of protein complexes in the yeast Saccharomyces cerevisiae , 2006, Nature.

[22]  Mike Tyers,et al.  BioGRID: a general repository for interaction datasets , 2005, Nucleic Acids Res..

[23]  K. N. Chandrika,et al.  Analysis of the human protein interactome and comparison with yeast, worm and fly interaction datasets , 2006, Nature Genetics.

[24]  Jun S. Liu,et al.  Bayesian inference of epistatic interactions in case-control studies , 2007, Nature Genetics.

[25]  Kenny Q. Ye,et al.  Strong Association of De Novo Copy Number Mutations with Autism , 2007, Science.

[26]  R. Redon,et al.  Relative Impact of Nucleotide and Copy Number Variation on Gene Expression Phenotypes , 2007, Science.

[27]  Manuel A. R. Ferreira,et al.  PLINK: a tool set for whole-genome association and population-based linkage analyses. , 2007, American journal of human genetics.

[28]  Joshua M. Korn,et al.  Association between microdeletion and microduplication at 16p11.2 and autism. , 2008, The New England journal of medicine.

[29]  Joseph A. Gogos,et al.  Strong association of de novo copy number mutations with sporadic schizophrenia , 2008, Nature Genetics.

[30]  C. Landry,et al.  An in Vivo Map of the Yeast Protein Interactome , 2008, Science.

[31]  P. Visscher,et al.  Rare chromosomal deletions and duplications increase risk of schizophrenia , 2008, Nature.

[32]  Joshua M. Korn,et al.  Association between microdeletion and microduplication at 16p11.2 and autism , 2008 .

[33]  Jason H. Moore,et al.  Exploiting the proteome to improve the genome-wide genetic analysis of epistasis in common human diseases , 2008, Human Genetics.

[34]  Yan V. Sun,et al.  Complexity in the genetic architecture of leukoaraiosis in hypertensive sibships from the GENOA Study , 2008, BMC Medical Genomics.

[35]  Joshua M. Korn,et al.  Integrated genotype calling and association analysis of SNPs, common copy number polymorphisms and rare CNVs , 2008, Nature Genetics.

[36]  Judy H Cho,et al.  Deletion polymorphism upstream of IRGM associated with altered IRGM expression and Crohn's disease , 2008, Nature Genetics.

[37]  P. Phillips Epistasis — the essential role of gene interactions in the structure and evolution of genetic systems , 2008, Nature Reviews Genetics.

[38]  A. Singleton,et al.  Rare Structural Variants Disrupt Multiple Genes in Neurodevelopmental Pathways in Schizophrenia , 2008, Science.

[39]  Judy H. Cho,et al.  Finding the missing heritability of complex diseases , 2009, Nature.

[40]  Yan V. Sun,et al.  A Common Copy Number Variation on Chromosome 6 Association With the Gene Expression Level of Endothelin 1 in Transformed B Lymphocytes From Three Racial Groups , 2009, Circulation. Cardiovascular genetics.

[41]  S. Gygi,et al.  Defining the Human Deubiquitinating Enzyme Interaction Landscape , 2009, Cell.

[42]  Scott M. Williams,et al.  Epistasis and its implications for personal genetics. , 2009, American journal of human genetics.

[43]  H. Cordell Detecting gene–gene interactions that underlie human diseases , 2009, Nature Reviews Genetics.

[44]  Jason H. Moore,et al.  Role for protein–protein interaction databases in human genetics , 2009, Expert review of proteomics.

[45]  Gregory A. Buck,et al.  Functional organization of the yeast proteome by a yeast interactome map , 2009, Proceedings of the National Academy of Sciences.

[46]  Jonathan Flint,et al.  Genetic architecture of quantitative traits in mice, flies, and humans. , 2009, Genome research.

[47]  Tim Becker,et al.  INTERSNP: genome-wide interaction analysis guided by a priori information , 2009, Bioinform..

[48]  Ariel S. Schwartz,et al.  An Atlas of Combinatorial Transcriptional Regulation in Mouse and Man , 2010, Cell.

[49]  Tomas W. Fitzgerald,et al.  Origins and functional impact of copy number variation in the human genome , 2010, Nature.

[50]  Gary D Bader,et al.  The Genetic Landscape of a Cell , 2010, Science.

[51]  M. Gerstein,et al.  Variation in Transcription Factor Binding Among Humans , 2010, Science.