Genetic variegation of clonal architecture and propagating cells in leukaemia

Little is known of the genetic architecture of cancer at the subclonal and single-cell level or in the cells responsible for cancer clone maintenance and propagation. Here we have examined this issue in childhood acute lymphoblastic leukaemia in which the ETV6–RUNX1 gene fusion is an early or initia...

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Published in	Nature (London) Vol. 469; no. 7330; pp. 356 - 361
Main Authors	Anderson, Kristina, Lutz, Christoph, van Delft, Frederik W., Bateman, Caroline M., Guo, Yanping, Colman, Susan M., Kempski, Helena, Moorman, Anthony V., Titley, Ian, Swansbury, John, Kearney, Lyndal, Enver, Tariq, Greaves, Mel
Format	Journal Article
Language	English
Published	London Nature Publishing Group UK 20.01.2011 Nature Publishing Group
Subjects	692/420/2489/144/68 692/699/67/1990/283/2125 Animals Artificial chromosomes Biological and medical sciences Cancer Cell cycle Clonal selection theory Clone Cells - metabolism Clone Cells - pathology Core Binding Factor Alpha 2 Subunit Disease Progression DNA Copy Number Variations - genetics DNA Mutational Analysis Genetic abnormalities Genetic aspects Genetic Variation - genetics Genetics Genotype Hematologic and hematopoietic diseases Humanities and Social Sciences Humans Immunophenotyping In Situ Hybridization, Fluorescence Interleukin Receptor Common gamma Subunit - deficiency Interleukin Receptor Common gamma Subunit - genetics Leukemia Leukemias. Malignant lymphomas. Malignant reticulosis. Myelofibrosis Medical sciences Mice Mice, Inbred NOD Mice, SCID multidisciplinary Mutation Neoplasm Transplantation Oncogene Proteins, Fusion - genetics Precursor Cell Lymphoblastic Leukemia-Lymphoma - genetics Precursor Cell Lymphoblastic Leukemia-Lymphoma - pathology Science Science (multidisciplinary) United Kingdom Human Variegation Propagation Lymphoproliferative syndrome Genetics Malignant hemopathy Genetic diversity Acute lymphocytic leukemia Cell Child Cancer Clone
Online Access	Get full text
ISSN	0028-0836 1476-4687 1476-4687
DOI	10.1038/nature09650

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Abstract	Little is known of the genetic architecture of cancer at the subclonal and single-cell level or in the cells responsible for cancer clone maintenance and propagation. Here we have examined this issue in childhood acute lymphoblastic leukaemia in which the ETV6–RUNX1 gene fusion is an early or initiating genetic lesion followed by a modest number of recurrent or ‘driver’ copy number alterations. By multiplexing fluorescence in situ hybridization probes for these mutations, up to eight genetic abnormalities can be detected in single cells, a genetic signature of subclones identified and a composite picture of subclonal architecture and putative ancestral trees assembled. Subclones in acute lymphoblastic leukaemia have variegated genetics and complex, nonlinear or branching evolutionary histories. Copy number alterations are independently and reiteratively acquired in subclones of individual patients, and in no preferential order. Clonal architecture is dynamic and is subject to change in the lead-up to a diagnosis and in relapse. Leukaemia propagating cells, assayed by serial transplantation in NOD/SCID IL2Rγ null mice, are also genetically variegated, mirroring subclonal patterns, and vary in competitive regenerative capacity in vivo . These data have implications for cancer genomics and for the targeted therapy of cancer. Genetic variation in leukaemia cells Genome-wide analysis of cancer cells in individual patients has revealed extensive genetic heterogeneity. Two groups have now mapped genetic homogeneity in patients with acute lymphoblastic leukaemia (ALL). Mel Greaves and colleagues obtained mutational profiles of large numbers of single cells from 60 individuals with ETV6 – RUNX1 -positive ALL, while John Dick and colleagues profile BCR-ABL1 -positive ALL. Both groups deduce the evolutionary path by which different subclones emerge during disease progression. Leukaemia-propagating cells that transplant the disease mirror the genetic variegation of the bulk tumours, providing insight into the heterogeneity of these functional subpopulations at the genetic level. This work has implications for therapeutic approaches targeting the tumours and specifically leukaemia-propagating cells. Analysing single cells from human B-cell acute lymphoblastic leukaemias, this study maps the genetic heterogeneity of cells within a given tumour sample, the evolutionary path by which different subclones have emerged, and ongoing dynamic changes associated with relapse. Leukaemia-propagating cells that transplant the disease mirror the genetic variegation of the bulk tumours, providing insights into the heterogeneity of these functional subpopulations at the genetic level. This has implications for therapeutic approaches targeting the tumours and specifically leukaemia-propagating cells.
AbstractList	Little is known of the genetic architecture of cancer at the subclonal and single-cell level or in the cells responsible for cancer clone maintenance and propagation. Here we have examined this issue in childhood acute lymphoblastic leukaemia in which the ETV6-RUNX1 gene fusion is an early or initiating genetic lesion followed by a modest number of recurrent or 'driver' copy number alterations. By multiplexing fluorescence in situ hybridization probes for these mutations, up to eight genetic abnormalities can be detected in single cells, a genetic signature of subclones identified and a composite picture of subclonal architecture and putative ancestral trees assembled. Subclones in acute lymphoblastic leukaemia have variegated genetics and complex, nonlinear or branching evolutionary histories. Copy number alterations are independently and reiteratively acquired in subclones of individual patients, and in no preferential order. Clonal architecture is dynamic and is subject to change in the lead-up to a diagnosis and in relapse. Leukaemia propagating cells, assayed by serial transplantation in NOD/SCID IL2Rγ(null) mice, are also genetically variegated, mirroring subclonal patterns, and vary in competitive regenerative capacity in vivo. These data have implications for cancer genomics and for the targeted therapy of cancer.Little is known of the genetic architecture of cancer at the subclonal and single-cell level or in the cells responsible for cancer clone maintenance and propagation. Here we have examined this issue in childhood acute lymphoblastic leukaemia in which the ETV6-RUNX1 gene fusion is an early or initiating genetic lesion followed by a modest number of recurrent or 'driver' copy number alterations. By multiplexing fluorescence in situ hybridization probes for these mutations, up to eight genetic abnormalities can be detected in single cells, a genetic signature of subclones identified and a composite picture of subclonal architecture and putative ancestral trees assembled. Subclones in acute lymphoblastic leukaemia have variegated genetics and complex, nonlinear or branching evolutionary histories. Copy number alterations are independently and reiteratively acquired in subclones of individual patients, and in no preferential order. Clonal architecture is dynamic and is subject to change in the lead-up to a diagnosis and in relapse. Leukaemia propagating cells, assayed by serial transplantation in NOD/SCID IL2Rγ(null) mice, are also genetically variegated, mirroring subclonal patterns, and vary in competitive regenerative capacity in vivo. These data have implications for cancer genomics and for the targeted therapy of cancer. Little is known of the genetic architecture of cancer at the subclonal and single-cell level or in the cells responsible for cancer clone maintenance and propagation. Here we have examined this issue in childhood acute lymphoblastic leukaemia in which the ETV6-RUNX1 gene fusion is an early or initiating genetic lesion followed by a modest number of recurrent or 'driver' copy number alterations. By multiplexing fluorescence in situ hybridization probes for these mutations, up to eight genetic abnormalities can be detected in single cells, a genetic signature of subclones identified and a composite picture of subclonal architecture and putative ancestral trees assembled. Subclones in acute lymphoblastic leukaemia have variegated genetics and complex, nonlinear or branching evolutionary histories. Copy number alterations are independently and reiteratively acquired in subclones of individual patients, and in no preferential order. Clonal architecture is dynamic and is subject to change in the lead-up to a diagnosis and in relapse. Leukaemia propagating cells, assayed by serial transplantation in NOD/SCID IL2RynuU mice, are also genetically variegated, mirroring subclonal patterns, and vary in competitive regenerative capacity in vivo. These data have implications for cancer genomics and for the targeted therapy of cancer. Little is known of the genetic architecture of cancer at the subclonal and single-cell level or in the cells responsible for cancer clone maintenance and propagation. Here we have examined this issue in childhood acute lymphoblastic leukaemia in which the ETV6-RUNX1 gene fusion is an early or initiating genetic lesion followed by a modest number of recurrent or 'driver' copy number alterations. By multiplexing fluorescence in situ hybridization probes for these mutations, up to eight genetic abnormalities can be detected in single cells, a genetic signature of subclones identified and a composite picture of subclonal architecture and putative ancestral trees assembled. Subclones in acute lymphoblastic leukaemia have variegated genetics and complex, nonlinear or branching evolutionary histories. Copy number alterations are independently and reiteratively acquired in subclones of individual patients, and in no preferential order. Clonal architecture is dynamic and is subject to change in the lead-up to a diagnosis and in relapse. Leukaemia propagating cells, assayed by serial transplantation in NOD/SCID IL2Rγ(null) mice, are also genetically variegated, mirroring subclonal patterns, and vary in competitive regenerative capacity in vivo. These data have implications for cancer genomics and for the targeted therapy of cancer. Little is known of the genetic architecture of cancer at the subclonal and single-cell level or in the cells responsible for cancer clone maintenance and propagation. Here we have examined this issue in childhood acute lymphoblastic leukaemia in which the ETV6-RUNX1 gene fusion is an early or initiating genetic lesion followed by a modest number of recurrent or 'driver' copy number alterations. By multiplexing fluorescence in situ hybridization probes for these mutations, up to eight genetic abnormalities can be detected in single cells, a genetic signature of subclones identified and a composite picture of subclonal architecture and putative ancestral trees assembled. Subclones in acute lymphoblastic leukaemia have variegated genetics and complex, nonlinear or branching evolutionary histories. Copy number alterations are independently and reiteratively acquired in subclones of individual patients, and in no preferential order. Clonal architecture is dynamic and is subject to change in the lead-up to a diagnosis and in relapse. Leukaemia propagating cells, assayed by serial transplantation in NOD/SCID IL2R gamma super(null) mice, are also genetically variegated, mirroring subclonal patterns, and vary in competitive regenerative capacity in vivo. These data have implications for cancer genomics and for the targeted therapy of cancer. Little is known of the genetic architecture of cancer at the subclonal and single-cell level or in the cells responsible for cancer clone maintenance and propagation. Here we have examined this issue in childhood acute lymphoblastic leukaemia in which the ETV6–RUNX1 gene fusion is an early or initiating genetic lesion followed by a modest number of recurrent or ‘driver’ copy number alterations. By multiplexing fluorescence in situ hybridization probes for these mutations, up to eight genetic abnormalities can be detected in single cells, a genetic signature of subclones identified and a composite picture of subclonal architecture and putative ancestral trees assembled. Subclones in acute lymphoblastic leukaemia have variegated genetics and complex, nonlinear or branching evolutionary histories. Copy number alterations are independently and reiteratively acquired in subclones of individual patients, and in no preferential order. Clonal architecture is dynamic and is subject to change in the lead-up to a diagnosis and in relapse. Leukaemia propagating cells, assayed by serial transplantation in NOD/SCID IL2Rγ null mice, are also genetically variegated, mirroring subclonal patterns, and vary in competitive regenerative capacity in vivo . These data have implications for cancer genomics and for the targeted therapy of cancer. Genetic variation in leukaemia cells Genome-wide analysis of cancer cells in individual patients has revealed extensive genetic heterogeneity. Two groups have now mapped genetic homogeneity in patients with acute lymphoblastic leukaemia (ALL). Mel Greaves and colleagues obtained mutational profiles of large numbers of single cells from 60 individuals with ETV6 – RUNX1 -positive ALL, while John Dick and colleagues profile BCR-ABL1 -positive ALL. Both groups deduce the evolutionary path by which different subclones emerge during disease progression. Leukaemia-propagating cells that transplant the disease mirror the genetic variegation of the bulk tumours, providing insight into the heterogeneity of these functional subpopulations at the genetic level. This work has implications for therapeutic approaches targeting the tumours and specifically leukaemia-propagating cells. Analysing single cells from human B-cell acute lymphoblastic leukaemias, this study maps the genetic heterogeneity of cells within a given tumour sample, the evolutionary path by which different subclones have emerged, and ongoing dynamic changes associated with relapse. Leukaemia-propagating cells that transplant the disease mirror the genetic variegation of the bulk tumours, providing insights into the heterogeneity of these functional subpopulations at the genetic level. This has implications for therapeutic approaches targeting the tumours and specifically leukaemia-propagating cells. Little is known of the genetic architecture of cancer at the subclonal and single-cell level or in the cells responsible for cancer clone maintenance and propagation. Here we have examined this issue in childhood acute lymphoblastic leukaemia in which the ETV6-RUNX1 gene fusion is an early or initiating genetic lesion followed by a modest number of recurrent or 'driver' copy number alterations. By multiplexing fluorescence in situ hybridization probes for these mutations, up to eight genetic abnormalities can be detected in single cells, a genetic signature of subclones identified and a composite picture of subclonal architecture and putative ancestral trees assembled. Subclones in acute lymphoblastic leukaemia have variegated genetics and complex, nonlinear or branching evolutionary histories. Copy number alterations are independently and reiteratively acquired in subclones of individual patients, and in no preferential order. Clonal architecture is dynamic and is subject to change in the lead-up to a diagnosis and in relapse. Leukaemia propagating cells, assayed by serial transplantation in NOD/SCID IL2Rγ^sup null^ mice, are also genetically variegated, mirroring subclonal patterns, and vary in competitive regenerative capacity in vivo. These data have implications for cancer genomics and for the targeted therapy of cancer. [PUBLICATION ABSTRACT]
Audience	Academic
Author	Lutz, Christoph van Delft, Frederik W. Moorman, Anthony V. Swansbury, John Kearney, Lyndal Bateman, Caroline M. Kempski, Helena Titley, Ian Anderson, Kristina Guo, Yanping Enver, Tariq Greaves, Mel Colman, Susan M.
Author_xml	– sequence: 1 givenname: Kristina surname: Anderson fullname: Anderson, Kristina organization: Section of Haemato-Oncology, The Institute of Cancer Research, Sutton SM2 5NG, UK – sequence: 2 givenname: Christoph surname: Lutz fullname: Lutz, Christoph organization: MRC Molecular Haematology Unit, Weatherall Institute of Molecular Medicine, John Radcliffe Hospital, Oxford OX3 9DS, UK – sequence: 3 givenname: Frederik W. surname: van Delft fullname: van Delft, Frederik W. organization: Section of Haemato-Oncology, The Institute of Cancer Research, Sutton SM2 5NG, UK – sequence: 4 givenname: Caroline M. surname: Bateman fullname: Bateman, Caroline M. organization: Section of Haemato-Oncology, The Institute of Cancer Research, Sutton SM2 5NG, UK – sequence: 5 givenname: Yanping surname: Guo fullname: Guo, Yanping organization: MRC Molecular Haematology Unit, Weatherall Institute of Molecular Medicine, John Radcliffe Hospital, Oxford OX3 9DS, UK – sequence: 6 givenname: Susan M. surname: Colman fullname: Colman, Susan M. organization: Section of Haemato-Oncology, The Institute of Cancer Research, Sutton SM2 5NG, UK – sequence: 7 givenname: Helena surname: Kempski fullname: Kempski, Helena organization: Paediatric Malignancy Unit, Great Ormond Street Hospital & UCL Institute of Child Health, London WC1N 3JH, UK – sequence: 8 givenname: Anthony V. surname: Moorman fullname: Moorman, Anthony V. organization: Leukaemia Research Cytogenetics Group, Northern Institute for Cancer Research, Newcastle University, Newcastle upon Tyne NE1 4LP, UK – sequence: 9 givenname: Ian surname: Titley fullname: Titley, Ian organization: Section of Haemato-Oncology, The Institute of Cancer Research, Sutton SM2 5NG, UK – sequence: 10 givenname: John surname: Swansbury fullname: Swansbury, John organization: Section of Haemato-Oncology, The Institute of Cancer Research, Sutton SM2 5NG, UK – sequence: 11 givenname: Lyndal surname: Kearney fullname: Kearney, Lyndal organization: Section of Haemato-Oncology, The Institute of Cancer Research, Sutton SM2 5NG, UK – sequence: 12 givenname: Tariq surname: Enver fullname: Enver, Tariq organization: MRC Molecular Haematology Unit, Weatherall Institute of Molecular Medicine, John Radcliffe Hospital, Oxford OX3 9DS, UK , Present address: University College London Cancer Institute, London WC1E 6BT, UK – sequence: 13 givenname: Mel surname: Greaves fullname: Greaves, Mel email: mel.greaves@icr.ac.uk organization: Section of Haemato-Oncology, The Institute of Cancer Research, Sutton SM2 5NG, UK
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ContentType	Journal Article
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Snippet	Little is known of the genetic architecture of cancer at the subclonal and single-cell level or in the cells responsible for cancer clone maintenance and...
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SubjectTerms	692/420/2489/144/68 692/699/67/1990/283/2125 Animals Artificial chromosomes Biological and medical sciences Cancer Cell cycle Clonal selection theory Clone Cells - metabolism Clone Cells - pathology Core Binding Factor Alpha 2 Subunit Disease Progression DNA Copy Number Variations - genetics DNA Mutational Analysis Genetic abnormalities Genetic aspects Genetic Variation - genetics Genetics Genotype Hematologic and hematopoietic diseases Humanities and Social Sciences Humans Immunophenotyping In Situ Hybridization, Fluorescence Interleukin Receptor Common gamma Subunit - deficiency Interleukin Receptor Common gamma Subunit - genetics Leukemia Leukemias. Malignant lymphomas. Malignant reticulosis. Myelofibrosis Medical sciences Mice Mice, Inbred NOD Mice, SCID multidisciplinary Mutation Neoplasm Transplantation Oncogene Proteins, Fusion - genetics Precursor Cell Lymphoblastic Leukemia-Lymphoma - genetics Precursor Cell Lymphoblastic Leukemia-Lymphoma - pathology Science Science (multidisciplinary)
Title	Genetic variegation of clonal architecture and propagating cells in leukaemia
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