Abstract
Pooled-DNA sequencing strategies enable fast, accurate, and cost-effect detection of rare variants, but current approaches are not able to accurately identify short insertions and deletions (indels), despite their pivotal role in genetic disease. Furthermore, the sensitivity and specificity of these methods depend on arbitrary, user-selected significance thresholds, whose optimal values change from experiment to experiment. Here, we present a combined experimental and computational strategy that combines a synthetically engineered DNA library inserted in each run and a new computational approach named SPLINTER that detects and quantifies short indels and substitutions in large pools. SPLINTER integrates information from the synthetic library to select the optimal significance thresholds for every experiment. We show that SPLINTER detects indels (up to 4 bp) and substitutions in large pools with high sensitivity and specificity, accurately quantifies variant frequency (r = 0.999), and compares favorably with existing algorithms for the analysis of pooled sequencing data. We applied our approach to analyze a cohort of 1152 individuals, identifying 48 variants and validating 14 of 14 (100%) predictions by individual genotyping. Thus, our strategy provides a novel and sensitive method that will speed the discovery of novel disease-causing rare variants.
MeSH Terms
Computational Biology/methods
Gene Frequency
Gene Library
Genotype
Humans
INDEL Mutation/genetics
Sensitivity and Specificity
Sequence Analysis, DNA/methods
Software
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Vallania Francesco L M
Center for Genome Sciences and Systems Biology, Department of Genetics, Washington University in St. Louis School of Medicine, St. Louis, Missouri 63108, USA.
Druley Todd E
Ramos Enrique
Wang Jue
Borecki Ingrid
Province Michael
Mitra Robi D
References (26)
26 references, click to expand
-
Methods for detecting associations with rare variants for common diseases: application to analysis of sequence data.
Am J Hum Genet. 2008 Sep;83(3):311-21
PMID: 18691683
-
DNA Sudoku--harnessing high-throughput sequencing for multiplexed specimen analysis.
Genome Res. 2009 Jul;19(7):1243-53
PMID: 19447965
-
Rare independent mutations in renal salt handling genes contribute to blood pressure variation.
Nat Genet. 2008 May;40(5):592-599
PMID: 18391953
-
Molecular heterogeneity of breast carcinomas and the cancer stem cell hypothesis.
Nat Rev Cancer. 2007 Oct;7(10):791-9
PMID: 17851544
-
A statistical method for the detection of variants from next-generation resequencing of DNA pools.
Bioinformatics. 2010 Jun 15;26(12):i318-24
PMID: 20529923
-
Common genetic variation and human traits.
N Engl J Med. 2009 Apr 23;360(17):1696-8
PMID: 19369660
-
Rare variant hypothesis for multifactorial inheritance: susceptibility to colorectal adenomas as a model.
Cell Cycle. 2005 Apr;4(4):521-5
PMID: 15753653
-
A small-cell lung cancer genome with complex signatures of tobacco exposure.
Nature. 2010 Jan 14;463(7278):184-90
PMID: 20016488
-
Multiple rare alleles contribute to low plasma levels of HDL cholesterol.
Science. 2004 Aug 6;305(5685):869-72
PMID: 15297675
-
Genetic variation in an individual human exome.
PLoS Genet. 2008 Aug 15;4(8):e1000160
PMID: 18704161
-
SNP discovery and allele frequency estimation by deep sequencing of reduced representation libraries.
Nat Methods. 2008 Mar;5(3):247-52
PMID: 18297082
-
On the allelic spectrum of human disease.
Trends Genet. 2001 Sep;17(9):502-10
PMID: 11525833
-
Medical sequencing at the extremes of human body mass.
Am J Hum Genet. 2007 Apr;80(4):779-91
PMID: 17357083
-
Mapping short DNA sequencing reads and calling variants using mapping quality scores.
Genome Res. 2008 Nov;18(11):1851-8
PMID: 18714091
-
Multiple rare variants in different genes account for multifactorial inherited susceptibility to colorectal adenomas.
Proc Natl Acad Sci U S A. 2004 Nov 9;101(45):15992-7
PMID: 15520370
-
The Human Gene Mutation Database: 2008 update.
Genome Med. 2009 Jan 22;1(1):13
PMID: 19348700
-
VarScan: variant detection in massively parallel sequencing of individual and pooled samples.
Bioinformatics. 2009 Sep 1;25(17):2283-5
PMID: 19542151
-
Quantification of rare allelic variants from pooled genomic DNA.
Nat Methods. 2009 Apr;6(4):263-5
PMID: 19252504
-
Experimental evolution of bet hedging.
Nature. 2009 Nov 5;462(7269):90-3
PMID: 19890329
-
The Sequence Alignment/Map format and SAMtools.
Bioinformatics. 2009 Aug 15;25(16):2078-9
PMID: 19505943
-
Finding the missing heritability of complex diseases.
Nature. 2009 Oct 8;461(7265):747-53
PMID: 19812666
-
Target-enrichment strategies for next-generation sequencing.
Nat Methods. 2010 Feb;7(2):111-8
PMID: 20111037
-
Breast and ovarian cancer risks due to inherited mutations in BRCA1 and BRCA2.
Science. 2003 Oct 24;302(5645):643-6
PMID: 14576434
-
Genome evolution and adaptation in a long-term experiment with Escherichia coli.
Nature. 2009 Oct 29;461(7268):1243-7
PMID: 19838166
-
Overlapping pools for high-throughput targeted resequencing.
Genome Res. 2009 Jul;19(7):1254-61
PMID: 19447964
-
Most pooling variation in array-based DNA pooling is attributable to array error rather than pool construction error.
Eur J Hum Genet. 2007 Apr;15(4):501-4
PMID: 17264871