A combinatorial approach for analyzing intra-tumor heterogeneity from high-throughput sequencing data

Motivation: High-throughput sequencing of tumor samples has shown that most tumors exhibit extensive intra-tumor heterogeneity, with multiple subpopulations of tumor cells containing different somatic mutations. Recent studies have quantified this intra-tumor heterogeneity by clustering mutations in...

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Published inBioinformatics (Oxford, England) Vol. 30; no. 12; pp. i78 - i86
Main Authors Hajirasouliha, Iman, Mahmoody, Ahmad, Raphael, Benjamin J.
Format Journal Article
LanguageEnglish
Published England Oxford University Press 15.06.2014
Subjects
Online AccessGet full text
ISSN1367-4803
1367-4811
1367-4811
DOI10.1093/bioinformatics/btu284

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Abstract Motivation: High-throughput sequencing of tumor samples has shown that most tumors exhibit extensive intra-tumor heterogeneity, with multiple subpopulations of tumor cells containing different somatic mutations. Recent studies have quantified this intra-tumor heterogeneity by clustering mutations into subpopulations according to the observed counts of DNA sequencing reads containing the variant allele. However, these clustering approaches do not consider that the population frequencies of different tumor subpopulations are correlated by their shared ancestry in the same population of cells. Results: We introduce the binary tree partition (BTP), a novel combinatorial formulation of the problem of constructing the subpopulations of tumor cells from the variant allele frequencies of somatic mutations. We show that finding a BTP is an NP-complete problem; derive an approximation algorithm for an optimization version of the problem; and present a recursive algorithm to find a BTP with errors in the input. We show that the resulting algorithm outperforms existing clustering approaches on simulated and real sequencing data. Availability and implementation: Python and MATLAB implementations of our method are available at http://compbio.cs.brown.edu/software/ Contact:  braphael@cs.brown.edu Supplementary information:  Supplementary data are available at Bioinformatics online.
AbstractList Motivation: High-throughput sequencing of tumor samples has shown that most tumors exhibit extensive intra-tumor heterogeneity, with multiple subpopulations of tumor cells containing different somatic mutations. Recent studies have quantified this intra-tumor heterogeneity by clustering mutations into subpopulations according to the observed counts of DNA sequencing reads containing the variant allele. However, these clustering approaches do not consider that the population frequencies of different tumor subpopulations are correlated by their shared ancestry in the same population of cells. Results: We introduce the binary tree partition (BTP), a novel combinatorial formulation of the problem of constructing the subpopulations of tumor cells from the variant allele frequencies of somatic mutations. We show that finding a BTP is an NP-complete problem; derive an approximation algorithm for an optimization version of the problem; and present a recursive algorithm to find a BTP with errors in the input. We show that the resulting algorithm outperforms existing clustering approaches on simulated and real sequencing data. Availability and implementation: Python and MATLAB implementations of our method are available at http://compbio.cs.brown.edu/software/ Contact: braphael@cs.brown.edu Supplementary information: Supplementary data are available at Bioinformatics online.
High-throughput sequencing of tumor samples has shown that most tumors exhibit extensive intra-tumor heterogeneity, with multiple subpopulations of tumor cells containing different somatic mutations. Recent studies have quantified this intra-tumor heterogeneity by clustering mutations into subpopulations according to the observed counts of DNA sequencing reads containing the variant allele. However, these clustering approaches do not consider that the population frequencies of different tumor subpopulations are correlated by their shared ancestry in the same population of cells. We introduce the binary tree partition (BTP), a novel combinatorial formulation of the problem of constructing the subpopulations of tumor cells from the variant allele frequencies of somatic mutations. We show that finding a BTP is an NP-complete problem; derive an approximation algorithm for an optimization version of the problem; and present a recursive algorithm to find a BTP with errors in the input. We show that the resulting algorithm outperforms existing clustering approaches on simulated and real sequencing data. Python and MATLAB implementations of our method are available at http://compbio.cs.brown.edu/software/ .
High-throughput sequencing of tumor samples has shown that most tumors exhibit extensive intra-tumor heterogeneity, with multiple subpopulations of tumor cells containing different somatic mutations. Recent studies have quantified this intra-tumor heterogeneity by clustering mutations into subpopulations according to the observed counts of DNA sequencing reads containing the variant allele. However, these clustering approaches do not consider that the population frequencies of different tumor subpopulations are correlated by their shared ancestry in the same population of cells.MOTIVATIONHigh-throughput sequencing of tumor samples has shown that most tumors exhibit extensive intra-tumor heterogeneity, with multiple subpopulations of tumor cells containing different somatic mutations. Recent studies have quantified this intra-tumor heterogeneity by clustering mutations into subpopulations according to the observed counts of DNA sequencing reads containing the variant allele. However, these clustering approaches do not consider that the population frequencies of different tumor subpopulations are correlated by their shared ancestry in the same population of cells.We introduce the binary tree partition (BTP), a novel combinatorial formulation of the problem of constructing the subpopulations of tumor cells from the variant allele frequencies of somatic mutations. We show that finding a BTP is an NP-complete problem; derive an approximation algorithm for an optimization version of the problem; and present a recursive algorithm to find a BTP with errors in the input. We show that the resulting algorithm outperforms existing clustering approaches on simulated and real sequencing data.RESULTSWe introduce the binary tree partition (BTP), a novel combinatorial formulation of the problem of constructing the subpopulations of tumor cells from the variant allele frequencies of somatic mutations. We show that finding a BTP is an NP-complete problem; derive an approximation algorithm for an optimization version of the problem; and present a recursive algorithm to find a BTP with errors in the input. We show that the resulting algorithm outperforms existing clustering approaches on simulated and real sequencing data.Python and MATLAB implementations of our method are available at http://compbio.cs.brown.edu/software/ .AVAILABILITY AND IMPLEMENTATIONPython and MATLAB implementations of our method are available at http://compbio.cs.brown.edu/software/ .
Motivation: High-throughput sequencing of tumor samples has shown that most tumors exhibit extensive intra-tumor heterogeneity, with multiple subpopulations of tumor cells containing different somatic mutations. Recent studies have quantified this intra-tumor heterogeneity by clustering mutations into subpopulations according to the observed counts of DNA sequencing reads containing the variant allele. However, these clustering approaches do not consider that the population frequencies of different tumor subpopulations are correlated by their shared ancestry in the same population of cells. Results: We introduce the binary tree partition (BTP), a novel combinatorial formulation of the problem of constructing the subpopulations of tumor cells from the variant allele frequencies of somatic mutations. We show that finding a BTP is an NP-complete problem; derive an approximation algorithm for an optimization version of the problem; and present a recursive algorithm to find a BTP with errors in the input. We show that the resulting algorithm outperforms existing clustering approaches on simulated and real sequencing data. Availability and implementation: Python and MATLAB implementations of our method are available at http://compbio.cs.brown.edu/software/ Contact:  braphael@cs.brown.edu Supplementary information:  Supplementary data are available at Bioinformatics online.
Author Mahmoody, Ahmad
Raphael, Benjamin J.
Hajirasouliha, Iman
AuthorAffiliation 1 Department of Computer Science and 2 Center for Computational Molecular Biology, Brown University, Providence, RI, 02906, USA
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Cites_doi 10.1016/j.cell.2012.04.023
10.1038/nature10933
10.1038/nature12213
10.1016/j.canlet.2012.12.028
10.1038/nmeth.2883
10.1038/nature09807
10.1186/1471-2105-15-35
10.1182/blood-2012-05-433540
10.1056/NEJMoa1113205
10.1126/science.959840
10.1038/nature10738
10.1186/gb-2013-14-7-r80
10.1137/0402008
10.1126/science.1235122
10.1038/nature12634
10.1016/j.cell.2012.02.025
10.1101/gr.151670.112
10.1038/nbt.2203
10.1016/j.cell.2012.02.028
10.1093/nar/gkt641
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References Xu (2023012711105044200_btu284-B25) 2012; 148
Shah (2023012711105044200_btu284-B22) 2012; 486
Oesper (2023012711105044200_btu284-B19) 2013; 14
Miller (2023012711105044200_btu284-B14)
Nowell (2023012711105044200_btu284-B18) 1976; 194
Salari (2023012711105044200_btu284-B20) 2013
Newburger (2023012711105044200_btu284-B16) 2013; 23
Ding (2023012711105044200_btu284-B3) 2013; 340
Jiao (2023012711105044200_btu284-B9) 2014; 15
Hou (2023012711105044200_btu284-B7) 2012; 148
Hurkens (2023012711105044200_btu284-B8) 1989; 2
Gerlinger (2023012711105044200_btu284-B5) 2012; 366
Kurihara (2023012711105044200_btu284-B12) 2006
Schuh (2023012711105044200_btu284-B21) 2012; 120
Nik-Zainal (2023012711105044200_btu284-B17) 2012; 149
Carter (2023012711105044200_btu284-B1) 2012; 30
Lawrence (2023012711105044200_btu284-B13) 2013; 499
Roth (2023012711105044200_btu284-B26) 2014; 11
Garey (2023012711105044200_btu284-B4) 1979
Strino (2023012711105044200_btu284-B23) 2013; 41
Navin (2023012711105044200_btu284-B15) 2011; 472
Ding (2023012711105044200_btu284-B2) 2012; 481
Vogelstein (2023012711105044200_btu284-B24) 2013; 339
Hajirasouliha (2023012711105044200_btu284-B6) 2007
Kandoth (2023012711105044200_btu284-B10) 2013; 502
23895164 - Genome Biol. 2013;14(7):R80
24633410 - Nat Methods. 2014 Apr;11(4):396-8
22495314 - Nature. 2012 Jun 21;486(7403):395-9
23539594 - Science. 2013 Mar 29;339(6127):1546-58
24484323 - BMC Bioinformatics. 2014;15:35
22397650 - N Engl J Med. 2012 Mar 8;366(10):883-92
22385958 - Cell. 2012 Mar 2;148(5):886-95
23770567 - Nature. 2013 Jul 11;499(7457):214-8
22608083 - Cell. 2012 May 25;149(5):994-1007
21399628 - Nature. 2011 Apr 7;472(7341):90-4
24195709 - J Comput Biol. 2013 Nov;20(11):933-44
24132290 - Nature. 2013 Oct 17;502(7471):333-9
23353056 - Cancer Lett. 2013 Nov 1;340(2):212-9
23892400 - Nucleic Acids Res. 2013 Sep;41(17):e165
22385957 - Cell. 2012 Mar 2;148(5):873-85
25102416 - PLoS Comput Biol. 2014 Aug 07;10(8):e1003665
22237025 - Nature. 2012 Jan 26;481(7382):506-10
23568837 - Genome Res. 2013 Jul;23(7):1097-108
959840 - Science. 1976 Oct 1;194(4260):23-8
22544022 - Nat Biotechnol. 2012 May;30(5):413-21
22915640 - Blood. 2012 Nov 15;120(20):4191-6
References_xml – start-page: 524
  volume-title: STACS
  year: 2007
  ident: 2023012711105044200_btu284-B6
  article-title: On completing latin squares
– volume: 149
  start-page: 994
  year: 2012
  ident: 2023012711105044200_btu284-B17
  article-title: The life history of 21 breast cancers
  publication-title: Cell
  doi: 10.1016/j.cell.2012.04.023
– volume: 486
  start-page: 395
  year: 2012
  ident: 2023012711105044200_btu284-B22
  article-title: The clonal and mutational evolution spectrum of primary triple-negative breast cancers
  publication-title: Nature
  doi: 10.1038/nature10933
– volume: 499
  start-page: 214
  year: 2013
  ident: 2023012711105044200_btu284-B13
  article-title: Mutational heterogeneity in cancer and the search for new cancer-associated genes
  publication-title: Nature
  doi: 10.1038/nature12213
– volume: 340
  start-page: 212
  year: 2013
  ident: 2023012711105044200_btu284-B3
  article-title: Advances for studying clonal evolution in cancer
  publication-title: Cancer Lett.
  doi: 10.1016/j.canlet.2012.12.028
– volume: 11
  start-page: 396
  year: 2014
  ident: 2023012711105044200_btu284-B26
  article-title: PyClone: statistical inference of clonal population structure in cancer
  publication-title: Nature Methods
  doi: 10.1038/nmeth.2883
– volume: 472
  start-page: 90
  year: 2011
  ident: 2023012711105044200_btu284-B15
  article-title: Tumour evolution inferred by single-cell sequencing
  publication-title: Nature
  doi: 10.1038/nature09807
– volume-title: Computers and Intractability: A Guide to the Theory of NP-Completeness
  year: 1979
  ident: 2023012711105044200_btu284-B4
– volume: 15
  start-page: 35
  year: 2014
  ident: 2023012711105044200_btu284-B9
  article-title: Inferring clonal evolution of tumors from single nucleotide somatic mutations
  publication-title: BMC Bioinformatics
  doi: 10.1186/1471-2105-15-35
– volume: 120
  start-page: 4191
  year: 2012
  ident: 2023012711105044200_btu284-B21
  article-title: Monitoring chronic lymphocytic leukemia progression by whole genome sequencing reveals heterogeneous clonal evolution patterns
  publication-title: Blood
  doi: 10.1182/blood-2012-05-433540
– volume: 366
  start-page: 883
  year: 2012
  ident: 2023012711105044200_btu284-B5
  article-title: Intratumor heterogeneity and branched evolution revealed by multiregion sequencing
  publication-title: N. Engl. J. Med.
  doi: 10.1056/NEJMoa1113205
– volume: 194
  start-page: 23
  year: 1976
  ident: 2023012711105044200_btu284-B18
  article-title: The clonal evolution of tumor cell populations
  publication-title: Science
  doi: 10.1126/science.959840
– start-page: 249
  volume-title: RECOMB
  year: 2013
  ident: 2023012711105044200_btu284-B20
  article-title: Inference of tumor phylogenies with improved somatic mutation discovery
– volume: 481
  start-page: 506
  year: 2012
  ident: 2023012711105044200_btu284-B2
  article-title: Clonal evolution in relapsed acute myeloid leukaemia revealed by whole-genome sequencing
  publication-title: Nature
  doi: 10.1038/nature10738
– ident: 2023012711105044200_btu284-B14
  article-title: Sciclone: Inferring clonal architecture and tracking the spatial and temporal patterns of tumor evolution
  publication-title: PLoS Comput Biol
– volume: 14
  start-page: R80
  year: 2013
  ident: 2023012711105044200_btu284-B19
  article-title: Theta: inferring intra-tumor heterogeneity from high-throughput dna sequencing data
  publication-title: Genome Biol.
  doi: 10.1186/gb-2013-14-7-r80
– volume: 2
  start-page: 68
  year: 1989
  ident: 2023012711105044200_btu284-B8
  article-title: On the size of systems of sets every t of which have an SDR, with an application to the worst-case ratio of heuristics for packing problems
  publication-title: SIAM J. Discret. Math.
  doi: 10.1137/0402008
– volume: 339
  start-page: 1546
  year: 2013
  ident: 2023012711105044200_btu284-B24
  article-title: Cancer genome landscapes
  publication-title: Science
  doi: 10.1126/science.1235122
– volume: 502
  start-page: 333
  year: 2013
  ident: 2023012711105044200_btu284-B10
  article-title: Mutational landscape and significance across 12 major cancer types
  publication-title: Nature
  doi: 10.1038/nature12634
– volume: 148
  start-page: 886
  year: 2012
  ident: 2023012711105044200_btu284-B25
  article-title: Single-cell exome sequencing reveals single-nucleotide mutation characteristics of a kidney tumor
  publication-title: Cell
  doi: 10.1016/j.cell.2012.02.025
– start-page: 761
  volume-title: NIPS
  year: 2006
  ident: 2023012711105044200_btu284-B12
  article-title: Accelerated variational dirichlet process mixtures
– volume: 23
  start-page: 1097
  year: 2013
  ident: 2023012711105044200_btu284-B16
  article-title: Genome evolution during progression to breast cancer
  publication-title: Genome Res.
  doi: 10.1101/gr.151670.112
– volume: 30
  start-page: 413
  year: 2012
  ident: 2023012711105044200_btu284-B1
  article-title: Absolute quantification of somatic DNA alterations in human cancer
  publication-title: Nat. Biotechnol.
  doi: 10.1038/nbt.2203
– volume: 148
  start-page: 873
  year: 2012
  ident: 2023012711105044200_btu284-B7
  article-title: Single-cell exome sequencing and monoclonal evolution of a JAK2-negative myeloproliferative neoplasm
  publication-title: Cell
  doi: 10.1016/j.cell.2012.02.028
– volume: 41
  start-page: e165
  year: 2013
  ident: 2023012711105044200_btu284-B23
  article-title: TrAp: a tree approach for fingerprinting subclonal tumor composition
  publication-title: Nucleic Acids Res.
  doi: 10.1093/nar/gkt641
– reference: 24633410 - Nat Methods. 2014 Apr;11(4):396-8
– reference: 959840 - Science. 1976 Oct 1;194(4260):23-8
– reference: 22608083 - Cell. 2012 May 25;149(5):994-1007
– reference: 24132290 - Nature. 2013 Oct 17;502(7471):333-9
– reference: 22495314 - Nature. 2012 Jun 21;486(7403):395-9
– reference: 23568837 - Genome Res. 2013 Jul;23(7):1097-108
– reference: 22237025 - Nature. 2012 Jan 26;481(7382):506-10
– reference: 23539594 - Science. 2013 Mar 29;339(6127):1546-58
– reference: 23770567 - Nature. 2013 Jul 11;499(7457):214-8
– reference: 22397650 - N Engl J Med. 2012 Mar 8;366(10):883-92
– reference: 22915640 - Blood. 2012 Nov 15;120(20):4191-6
– reference: 23892400 - Nucleic Acids Res. 2013 Sep;41(17):e165
– reference: 22544022 - Nat Biotechnol. 2012 May;30(5):413-21
– reference: 24195709 - J Comput Biol. 2013 Nov;20(11):933-44
– reference: 25102416 - PLoS Comput Biol. 2014 Aug 07;10(8):e1003665
– reference: 23353056 - Cancer Lett. 2013 Nov 1;340(2):212-9
– reference: 22385957 - Cell. 2012 Mar 2;148(5):873-85
– reference: 24484323 - BMC Bioinformatics. 2014;15:35
– reference: 21399628 - Nature. 2011 Apr 7;472(7341):90-4
– reference: 23895164 - Genome Biol. 2013;14(7):R80
– reference: 22385958 - Cell. 2012 Mar 2;148(5):886-95
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Snippet Motivation: High-throughput sequencing of tumor samples has shown that most tumors exhibit extensive intra-tumor heterogeneity, with multiple subpopulations of...
High-throughput sequencing of tumor samples has shown that most tumors exhibit extensive intra-tumor heterogeneity, with multiple subpopulations of tumor cells...
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SubjectTerms Algorithms
Cluster Analysis
Gene Frequency
High-Throughput Nucleotide Sequencing
Humans
Ismb 2014 Proceedings Papers Committee
Leukemia, Myeloid, Acute - genetics
Mutation
Neoplasms - genetics
Sequence Analysis, DNA
Title A combinatorial approach for analyzing intra-tumor heterogeneity from high-throughput sequencing data
URI https://www.ncbi.nlm.nih.gov/pubmed/24932008
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https://pubmed.ncbi.nlm.nih.gov/PMC4058927
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